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Infect Immun, May 1998, p. 2128-2134, Vol. 66, No. 5
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Kinetics of Infection and Effects on Placental Cell Populations
in a Murine Model of Chlamydia psittaci-Induced
Abortion
Antonio J.
Buendía,1,*
Joaquín
Sánchez,2
María C.
Martínez,2
Paulina
Cámara,2
Jose
A.
Navarro,2
Annie
Rodolakis,3 and
Jesus
Salinas1
Departamento de Patología Animal
(Microbiología e Inmunología)1
and
Departamento de Histología y Anatomía
Patológica,2 Facultad de Veterinaria,
Universidad de Murcia, 30100 Murcia, Spain, and
Pathologie
Infectiouse et Immunologie, Institut National de la Recherche
Agronomique, 37380 Nouzilly, France3
Received 14 November 1997/Returned for modification 30 December
1997/Accepted 13 February 1998
 |
ABSTRACT |
The anatomical progression of chlamydial infection was studied in
different areas of the placenta, using a mouse model and two
inoculation times: early pregnancy (day 7, group A) and midpregnancy (day 11, group B). The first population cells affected were decidual cells and neutrophils located just at the limits of the
maternal and fetal placenta. The following invaded area was the
layer of giant cells. Complete colonization of the maternal placenta
occurred after day 15 of pregnancy independently of the inoculation
time, the metrial gland being the last area to be invaded; numerous granulated metrial gland (GMG) cells were infected. Finally,
chlamydial inclusions were observed in labyrinthine trophoblastic cells
from day 18 of pregnancy onward. Since no fetal damage was observed, it
seems that an indirect mechanism involving the lysis of GMG cells
and neutrophil infiltration of the decidua and metrial gland may be the pathogenic mechanism that leads to abortion.
| |
INTRODUCTION |
Chlamydia psittaci
serotype 1 is an obligate intracellular bacterium which can colonize
very different types of placenta (ruminant, porcine, human, and
murine), causing abortion during the last third of the gestation
period. The disease is especially important in small ruminants, the
natural hosts of the bacterium, because of the economic losses it
causes. However, the bacteria also present a potential zoonotic risk to
pregnant women, since several cases of human abortion followed
by severe complications have been reported after exposure to goats or
sheep in abattoirs or during lambing (11, 13, 28).
Chlamydiae show a unique growth cycle (17): infection begins
with adhesion of an infectious elementary body (EB) to a susceptible cell, followed by phagocytosis within a phagosome. The EB is
transformed into an active metabolic form, the reticulate body
(RB), which divides by binary fission. The cycle ends with
reorganization of RBs into EBs and the release of EBs, causing
infection in nearby cells.
Previously we developed a model of chlamydial infection in pregnant
mice (7, 21), in which intraperitoneal or intravenous inoculation with 105 to 106 PFU of C. psittaci serotype 1 caused abortion, usually by day 19 or 20 of
pregnancy in nearly all of the pregnant mice inoculated. These
late-term abortions appeared similar to those observed in cases of
natural or experimentally induced abortion in small ruminants. In fact,
this model has already been used to control the efficacy of commercial
vaccines (20) and antigens suitable for vaccine development
(10) or to measure the virulence of different strains (7, 21). In a preliminary study (23), we showed
that C. psittaci infect the granulated metrial gland
(GMG) cells, a lymphoid cell population, related to NK cells (18,
24), that are located during pregnancy mainly in the metrial
gland and in the decidua basalis. These cells are the major lymphoid
population associated with pregnancy. Their function is not clearly
understood but, like their morphology, seems to vary during
pregnancy. A putative defensive function against intracellular
pathogens has been proposed (29), since these
cells contain granules with cytotoxic molecules (perforins and serine
esterases). Whatever the case may be, their functionality and number
seem to decrease from day 15 of pregnancy onward (8, 9).
Recently, several studies using different placental pathogens have been
performed to show how the inoculation time influences the outcome of
pregnancy (1, 2, 5, 16). However, there has been no
description of the different areas of the placenta invaded by pathogens
according to the time of infection, nor has it been observed whether
these pathogens are able to invade GMG cells.
The aim of this work was to study which of the placental areas and cell
populations are invaded by C. psittaci in an attempt to
clarify the pathological mechanisms that cause abortion and to see
whether there was any relationship with the time that inoculation was
carried out.
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MATERIALS AND METHODS |
Microorganism.
The AB7 strain (21) of C. psittaci serotype 1 used in this study was isolated from an ovine
abortion and was propagated in chicken embryo yolk sac in our
laboratory. Chlamydiae were titered by a modification of the
plaque-forming technique (3) on McCoy cells and stored at
80°C until use.
Mice.
Adult (56- to 60-day-old) OF1 mice (outbred) were
obtained from the animal facility of the Institut de la Recherche
Agronomique, Nouzilly, France. Virgin females were mated with males of
the same strain. The presence of a vaginal plug was designated day 0 of
pregnancy. The mice were then placed in individual cages and weighed
daily.
Experimental design.
To evaluate the role of the time of
inoculation in the development of chlamydial infection, the mice were
divided into two groups: group A, consisting of mice inoculated at day
7 of pregnancy (early pregnancy), and group B, inoculated at day 11 of
pregnancy (midpregnancy). Inoculation was carried out intraperitoneally with 5 × 105 PFU of C. psittaci in 0.2 ml
of 0.1 M phosphate-buffered saline (PBS). Mice were killed at days 3, 5, 7, 9, 11, 13, 15, 17, and 21 postinfection (p.i.), four or more mice
being sacrificed each time. Samples from the liver, spleen, and
different areas of placenta were processed after necropsy for both
light and electron microscopy. The control group consisted of 10 pregnant but uninoculated mice.
Immunohistochemistry.
Samples were collected and stained by
the avidin-biotin-peroxidase complex (ABC) and immunogold techniques as
previously described (23). Briefly, fetoplacental units from
the mice were fixed in 10% formaldehyde in PBS, dehydrated, and
embedded in paraffin wax at 56°C for light microscopy. To visualize
chlamydial antigen on paraffin sections (5 µm), immunohistochemical
staining was carried out with a biotinylated mouse monoclonal
anti-chlamydial lipopolysaccharide (LPS) antibody (22)
(dilution, 1:25), and the ABC according to the instructions of the
manufacturer (Vector Laboratories, Burlingame, Calif.). A positive
reaction was demonstrated by the precipitation of diaminobenzidine
tetrahydrochloride. Sections were subsequently stained with hematoxylin
or with the periodic acid-Schiff technique.
For electron microscopy, fetoplacental units were rapidly excised and
immersed in a mixture of 2% paraformaldehyde and 1% glutaraldehyde in
0.1 M PBS. The metrial gland, decidua basalis, and labyrinth were cut
into small pieces and fixed in the same fixative for 24 h at
4°C. After fixation, the tissues were dehydrated in ethanol and
embedded in LR-White resin, soft grade (London Resin Company,
Basingstoke, England). Thick sections (1 µm) were cut, stained with
toluidine blue, and examined with the light microscope to locate the
infected cells. Ultrathin sections (80 nm) were then cut and
immunostained with the biotinylated anti-chlamydial LPS monoclonal
antibody described above (dilution, 1:25) as previously described
(22). Briefly, sections were collected on nickel grids and
incubated for 1 h at 37°C with the primary biotinylated anti-LPS antibody. After several washes in PBS, the sections were incubated for
30 min at 37°C with streptavidin-gold (10 nm) (Sigma, Madrid, Spain),
then washed in PBS, and counterstained in aqueous uranyl acetate and
lead citrate.
Control sections were reacted by the ABC or immunogold technique. These
control sections either were treated with nonimmune
mouse serum instead
of the primary antibody or were sections of
tissue from noninfected
mice. The control sections were all negative.
Statistical analysis.
The mean and standard deviation were
calculated for each group of animals. Nonparametric tests (Mann-Whitney
U test) were used to compare differences between groups A and B. Results were considered significant when P was <0.05.
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RESULTS |
Pregnancy outcome.
All the pregnant mice inoculated, if not
previously sacrificed, aborted at days 19 to 20 of pregnancy (12 to 13 days p.i. for group A; 8 to 9 days p.i. for group B), while the
noninoculated control group had an average litter of 12 live baby mice
at days 21 to 22 of pregnancy.
Early stages of the infection.
In our model, which involved
intraperitoneal inoculation, the placenta was not the primary target
organ of C. psittaci, since positive immunoreaction was not
detected until day 5 p.i. in the mice of group A and was detected
only in some mice of group B at day 3 p.i. However, the spleen and
liver of mice in both groups showed moderate immunoreaction at day
3 p.i. (data not shown). The first placental area to be colonized
by C. psittaci was the decidua basalis, at the very limit of
the giant cells layer (day 3 in group B; day 5 in group A), where
chlamydial inclusion in decidual cells and immunolabelled neutrophils
could be observed, always near maternal vessels.
Progression of the infection.
Progression of the infection
depended on the day of inoculation (Tables
1 and 2).
In group A it was quite slow: at day 5 p.i. (Fig.
1a), chlamydial antigen could be seen in
the decidua basalis and decidua parietalis, decidual cells and
neutrophils being the cell populations affected. Electron microscopy
showed the decidual cells to have classical chlamydial inclusions,
while the neutrophils continued to change as infection progressed in both groups. During the first stages of infection, the neutrophils contained immunolabelled remains that suggested a successful phagocytic function (Fig. 2a), while in more
advanced stages they showed condensation of the nuclear chromatin and
numerous EBs (Fig. 2b), reflecting a breakdown in the control of the
infection. No sign of active chlamydial reproduction was observed in
neutrophils (typical inclusions with RBs and EBs).
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TABLE 1.
Distribution and intensity of the immunoreaction to
C. psittaci antigen in the uterus, maternal placenta, fetal
placenta, and fetus of mice inoculated on day 7 of
pregnancy (group A)
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TABLE 2.
Distribution and intensity of the immunoreaction to
C. psittaci antigen in the uterus, maternal placenta,
fetal placenta, and fetus of mice inoculated on day 11 of
pregnancy (group B)
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FIG. 1.
Paraffin wax sections immunostained by the ABC method
showing the distribution of positive immunoreaction (arrowheads and
asterisks) in the placental areas. Notice that the anatomical
progression of infection was increased in group B with regard to group
A. (a to c) Group A at 5 days p.i. (small focus in the decidua basalis
next to giant-cell layer), 7 days p.i. (small foci disseminated in the
decidua basalis), and 9 days p.i. (immunoreaction foci spread through
the metrial gland), respectively. (d to f) Group B at 5 days p.i.
(small foci disseminated in the decidua basalis and metrial gland), 7 days p.i. (foci forming extensive immunoreaction areas in the decidua
basalis and metrial gland), and 9 days p.i. (very extensive
immunoreaction area occupying decidua basalis and metrial gland
[asterisk] and immunoreaction foci spread through the labyrinth
[arrowhead]), respectively. Bar, 266.6 µm for all photographies.
MG, metrial gland; D, decidua basalis; L, labyrinth.
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FIG. 2.
Electron photomicrographs of the different cell
populations affected by chlamydial infection labelled by the immunogold
technique. (a) Neutrophil with remains of immunolabelled material
within phagolysosomes, day 14 of pregnancy (7 p.i.). Bar, 1.66 µm.
(b) Neutrophils with degenerative changes and chromatin condensation
containing numerous EBs, day 18 of pregnancy (11 p.i.). Bar, 1.66 µm.
(c) Giant cell with a chlamydial inclusion, day 14 of pregnancy (7 p.i.). Bar, 1.98 µm. (d) GMG cell with a young chlamydial inclusion,
day 16 of pregnancy (9 p.i.). Bar, 2.64 µm. (e) Decidual cell with a
very large chlamydial inclusion, day 18 of pregnancy (11 p.i.). Bar,
1.51 µm.
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By day 7 p.i. (Fig.
1b), the decidua capsularis had also been
colonized and very large inclusions appeared in the giant-cell
layer
(Fig.
2c), although no immunoreaction was found in the metrial
gland.
At day 9 p.i. (Fig.
1c), weak immunoreaction was observed
in the
metrial gland whereas the decidua basalis showed moderate
reaction,
some GMG cells showing chlamydial inclusions in both
areas (Fig.
2d).
At day 11 p.i., the immunoreaction was moderate
in the metrial
gland and strong in the decidua basalis, with many
GMG cells infected.
There were very large inclusions in the decidual
cells (Fig.
2e) and a
high degree of neutrophil infiltration of
both areas. In the labyrinth,
some inclusions were observed in
trophoblast cells and also
immunolabelled neutrophils in small
foci. By day 13 p.i., some
mice of group A had aborted. These
mice showed a strong immunoreaction
in the sites of previous attachment
(Fig.
3a) and also in the uterus
lumen, this positive immunoreaction
remaining until day 17 p.i.
Immunoreaction was not detected at
day 21 p.i. Electron microscopy
(Fig.
3b) showed that the immunoreaction
was localized in the debris of necrotic cells, in degenerated
neutrophils, and in extracellular groups of EBs. The decidua basalis
and metrial gland of the mice that had not aborted showed an image
similar to that at day 11 p.i., with substantial infiltration
of
neutrophils.
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FIG. 3.
Site of previous attachment at day 2 postabortion. (a)
Paraffin wax section immunostained by the ABC technique. Bar, 266.6 µm. (b) Electron photomicrograph labelled by the immunogold
technique, showing groups of EBs, amorphous immunolabelled material,
and cells with significant degenerative changes. Bar, 1.66 µm.
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In group B, the anatomical progression of the infection was noticeably
faster (Table
2). By day 5 p.i. (Fig.
1d), the metrial
gland
already showed immunoreaction and several GMG cells both
in the decidua
basalis and metrial gland were infected. The giant-cell
layer was also
invaded. At day 7 p.i. (Fig.
1e), the metrial gland
and decidua
basalis showed a strong immunoreaction, with substantial
neutrophilic
infiltration as well as numerous decidual and GMG
cells with chlamydial
inclusions. The infection stage was the
equivalent to that at day 11 for group A; there were not significant
differences in the
immunoreaction (
P < 0.05). Likewise, day 9
p.i.
(Fig.
1f) was the equivalent of day 13 in group A, both in
aborted and
in nonaborted mice. The positive immunoreaction in
the site of previous
placental attachment remained in this group
until day 15 p.i.
Immunoreaction was not detected at day 17 or
21 p.i.
There was no sign of immunoreaction in any fetus or of
histopathological lesions in either group A or group B.
| |
DISCUSSION |
The first placental area to be invaded by C. psittaci
was the boundary between the maternal and fetal placenta, which was previously identified as the first center of infection in the placenta
for different intracellular bacteria such as Coxiella burnetii (4), Listeria monocytogenes
(19), and Brucella abortus (26). This
border area between the maternal and fetal placenta is a suitable place
for intracellular pathogen settlement since there are very few or no
maternal macrophages or T cells to facilitate the survival of the fetal
trophoblast (19). Neutrophils were the only defensive cell
population which reached the decidua to any great extent as late as
13 p.i., by which time in the liver and spleen of the same animals
they partially had been replaced by macrophages beginning on day 5 p.i. (data not shown). However, the neutrophils were unable to control
chlamydial replication, while their massive accumulation,
degeneration, and lysis could cause significant necrosis in the
decidua. Neutrophil infiltration and extensive necrosis of the
maternal-fetal junctions is a characteristic event of chlamydial
infection of ruminant placenta (6), and similar lesions have
been observed in several cases of gestational chlamydiosis in human
beings, involving acute inflammatory cells in the intervillous spaces
together with inflammation of the decidual bed (13, 28).
Extensive neutrophil infiltration has been observed in murine placental
infection with other intracellular pathogens such as Coxiella
burnetii (4), L. monocytogenes
(19), and B. abortus (26).
A comparison of the rate at which infection developed in both groups
indicated a delay of 4 days in group A; the metrial gland was not
susceptible to chlamydia infection until day 15 of pregnancy regardless
of the time of inoculation, this moment of pregnancy coinciding with
the time at which the GMG cells start to lose their functionality
(8). This fact suggests that the ability of chlamydiae to
infect these cells and to completely colonize the maternal placenta
depends on the functional state of the GMG cells. It has been suggested
that the composition and increased granularity of the mature GMG cells
accompanied by cell death may be a part of a mechanism to facilitate
separation of the placenta from the uterine wall at parturition
(8, 25), while the chlamydia-induced lysis of GMG cells and
the release of their granules could contribute to a premature placental
separation at abortion. In sheep, despite the differences in the type
of placenta and local immune response in relation to mouse, it is well
known that endometrial tissues contain cells which are morphologically
and functionally analogous to the GMG cells of pregnant rodent uterus
although they are 
TCR+ CD8+
(12). However, it is not known whether these cells develop NK activity. During pregnancy, this large granulated lymphocyte subpopulation increases in the lumimal epithelium in the
interplacentomal endometrium and may represent up to 10% of the cells
of this tissue (15). In pregnant human uterus, large
granulated lymphocytes have been identified as a subset of NK cells in
the decidua (14) and seem to be related to GMG cells. The
role of these cell populations in chlamydial infection of ruminant or
human placenta has not been determined.
In our experiments there was no sign of immunoreaction in any fetus or
of any histopathological findings, which suggests that chlamydiae do
not directly damage the fetus. However, Rodolakis et al.
(21) isolated chlamydiae from the fetus by the
plaque-forming method, although in very low numbers (103-
to 105-fold less than in placenta). This apparent
disagreement could be due to the poor sensitivity of the
immunohistochemical technique, since it may be able to detect easily
chlamydial inclusions but not scarce free EBs. In our model, chlamydiae
probably reached the fetus from day 18 of pregnancy, when the labyrinth
was invaded, although they did not have time to cause lesions since
abortion occurred on days 19 to 20. In sheep, chlamydiae also reach the fetus during the last third of pregnancy, causing focal necrosis in the
liver and other organs (6). However, in this case the time
elapsing between fetal infection and abortion is greater (about 30 days). In chlamydial human abortion, on the other hand, although
bacteria were isolated from both fetal and placental tissue,
histopathological changes were observed only in the placenta (28). The murine model therefore is quite similar to human
chlamydial abortion.
A very similar occurrence has been observed with Coxiella
burnetii, where hepatic lesions have been found in fetus from
naturally infected sheep (27); however,
Baumgärtner and Bachmann in an extensive immunohistochemical
study (4) found no positive immunoreaction or lesions in the
fetuses of experimentally infected pregnant mice but found both lesions
and positive immunoreaction in surviving 9-day-old offspring, which
suggests that fetal infection occurred just before or after birth.
In conclusion, our findings suggest that there is no important damage
to the fetus prior to abortion, although two occurrences that could
represent an indirect form of damage to the fetus took place in the
decidua basalis: lysis of GMG cells with the subsequent release of
granules containing cytotoxic proteins and pronounced infiltration of
this area by neutrophils. Both of these occurrences, together with the
direct destruction of the decidual cells by chlamydiae, could lead to a
malfunctioning of the maternal placenta and a premature breaking of the
decidua basalis, coinciding with the late-term abortion induced by
chlamydiae.
| |
ACKNOWLEDGMENTS |
This work was supported in part by Comisión
Interministerial de Ciencia y Tecnología (CICYT) grant
AGF97-0459. A. J. Buendía was the recipient of a
predoctoral grant from the Universidad de Murcia, Murcia, Spain.
We thank Ian J. Stewart for helpful suggestions at the outset of this
study and A. Souriau for help in the biotinylation of the
antichlamydial monoclonal antibody.
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FOOTNOTES |
*
Corresponding author. Mailing address: Departamento
Patología Animal (Microbiología e Inmunología),
Facultad de Veterinaria, Universidad de Murcia, Campus de
Espinardo, Murcia 30100, Spain. Phone: (34) 68 364810. Fax: (34)
68 364147. E-mail: abuendia{at}fcu.um.es.
Editor: J. G. Cannon
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Infect Immun, May 1998, p. 2128-2134, Vol. 66, No. 5
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
