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Quantitative analysis of zonulae occuldentes between oviductal epithelial cells at diestrous and estrous stages in the mouseFreeze-fracture study.

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THE ANATOMICAL RECORD 206:257-266 (1983)
Quantitative Analysis of Zonulae Occludentes Between
Oviductal Epithelial Cells at Diestrous and Estrous
Stages in the Mouse: Freeze-Fracture Study
KIYOTAKA TOSHIMORI, RUIKO HIGASHI,
AND
CHIKAYOSHI GURA
Department ofAnatom y, Medical College of Myazakz, Mzyazakl,
Japan 889-16
ABSTRACT
The zonulae occludentes between oviductal epithelial cells
were quantitatively analyzed at diestrous and estrous stages in the mouse,
using the freeze-fracture technique. Zonulae occludentes were predominantly
anastomosing a t the diestrous stage, while they were predominantly parallel
a t the estrous stage. The lowest mean value of junctional strands comprising
the zonulae occludentes was 5.3 rt 1.6. Parallel-type zonulae occludentes had
more strands than the anastomosing type. Secretory cells usually had more
strands than ciliated cells. The shallowest mean depth occupied by junctional
domain was 0.51 k 0.20 pm. The depth was usually somewhat greater in
anastomosing-type zonulae occludentes than in the parallel type. It was also
slightly greater in ciliated cells than in secretory cells. The depth was likely to
be greater a t diestrous stage than a t the estrous stage. However, neither the
number of strands nor the depth was significantly different between diestrous
and estrous stages in homologous types of zonulae occludentes. On the basis of
these results, the zonulae occludentes in oviductal epithelium are considered
to be morphologically of a tight type a t any time period throughout the estrous
cycle. The results of lanthanum tracer experiments suggest that the zonulae
occludentes in the oviductal epithelium do not; always function as a barrier to
the exogenous tracer.
These morphological phenomena are discussed in relation to mouse fertilization in vivo.
The mammalian oviduct is customarily
subdivided into three regions, isthmus, ampulla, and fimbriated infundibulium. In the
tract, secretory cells (nonciliated) and ciliated cells are the primary types. Secretory
cells are more abundant than ciliated cells in
the isthmus, while the proportion of secretory cells decreases gradually from the isthmus to the ampulla. Such regional variations
of the lining epithelium are well known (Clyman, 1966; Hafez, 1973).
The response of the mammalian oviducts
to the ovarian hormones (estrogen and progesterone) is also well known (Clyman, 1966;
Beier, 1974; West et al., 1976; Komatsu and
Fujita, 1978; Verhage et al., 1979; Odor et al.,
1980; Bareither and Verhage, 1981). These
hormonal changes regulate the amount and
composition of the oviductal luminal fluid
(Urzua et al., 1970; Blandau, 1971; Beier,
r
1983 ALAN R LISS, INC
1974). The distended oviductal lumen contains fluid, conspicuously in the ampulla,
which is rapidly accumulated under the influence of estrogen at the estrous stage. Progesterone causes closure of the oviductal
lumen and resorption of luminal fluid at the
diestrous stage.
No detailed report has been published on
freeze-fracture images of the oviductal epithelium, although Komatsu et al. (1979) reported two types of zonulae occludentes
between adjacent epithelial cells in the
mouse; i.e., parallel (few anastomosing) and
anastomosing types. However, they did not
mention regional differences in the distribution of zonulae occludentes in the oviduct
during the estrous cycle.
Received December 9,1982; accepted March 15, 1983.
258
K. TOSHIMOKI, R. HIGASHI, AND c. ~ U R A
In general, zonulae occludentes function as
a diffusion barrier to separate the internal
environment of the body from the external
world (Farquhar and Palade, 1963; Reese and
Karnovsky, 1967; Claude and Goodenough,
1973; Staehelin, 1974). We were, therefore,
interested in examining how the zonulae occludentes between oviductal epithelial cells
are organized a t the time of fertilization, and
whether there is a difference in the structure
of the zonulae occludentes between the diestrous and estrous stages. A preliminary report of this work has appeared elsewhere
(Toshimori et al., 1982).
(diestrous stage) of the same strain at room
temperature. The various regions of the oviduct were selected and cut into small pieces.
The tissues were then postfixed with 2% osmium tetroxide in the same buffer described
above. After dehydration by ethanol as usual,
they were embedded in Epon 812. The sections were cut by a glassknife-equipped LKB
ultrotome and stained with uranyl acetate.
The replicas and thin sections were examined by JEOL 100B or 200CX electron microscopes at a n accelerating voltage of 80 kV.
Quantitation for Zonulae Occludentes
Ten animals were used for control oviducts
MATERIALS AND METHODS
a t the diestrous stage and 30 for the isthmus
Freeze-Fracture
and ampulla at the estrous stage. Fifty zonMale and female ddY strain mice, 6-12 ulae occludentes analyzable on cleaved
weeks in age, were housed in a controlled planes were selected from each of secretory
environment (7 AM - 7 PM:light; 7 PM - 7 AM: and ciliated cells in the control oviducts, and
dark) and provided with food and water ad the isthmus and ampulla at the estrous stage.
libitum. The females were induced to ovulate Therefore, the total number of zonulae occluwith a n intraperitoneal injection of 2 IU of dentes examined was 300. The following
pregnant mare’s serum (PMS),followed by 2 characteristics of zonulae occludentes were
IU of human chorionic gonadotropin (HCG), analyzed: 1) the number of zonulae occlu48 hours later. Such doses usually induced dentes with parallel or anastomosing type
1-20 eggs in the ampulla of each oviduct as (classification of the junctional type is depreviously reported by one of the authors scribed in Results), 2) the number of junc(Toshimori, 1982). They were mated with the tional strands, and 3) the depth along the
males and sacrificed by cervical dislocation lateral plasma membrane occupied by junca t 0.5-3 hours after plug formation (10-15 tional strands. Analyses were made only in
hours after HCG injection). Reproductive or- micrographs where junctions were exposed
gans were dissected out into 2.5% glutaral- from apical to basal edge. Measurements for
dehyde adjusted to pH 7.2 by 0.1 M cacodylate the second and third characteristics were
buffer a t room temperature. The oviduct was made of the average number of strands and
clearly divided into two regions, isthmus and of the average depth of a n exposed junction,
ampulla. As a control for the diestrous stage respectively. These analytical data were ex(control oviduct), female mice were used in pressed as mean standard deviation of the
which about 60 hours had elapsed after HCG mean (SD). Differences were assessed by x2injection. At this time, the boundary between test for the first characteristic and by Stuisthmus and ampulla (I-Ajunction) could not dent’s t-test for the second and third characbe clearly identified by stereoscope, since the teristics. P < .05 was used as indicating a
lumen of the oviduct had already been re- significant difference.
duced. Therefore, the control oviduct conRESULTS
tained either isthmus only or both isthmus
and ampulla. They were dissected and fixed
The word “control oviduct” is used only for
in the same manner described above. These the diestrous stage, while the words “isthsamples were then cryoprotected by 30% mus” and “ampulla” are used only for the
glycerin overnight. The replicas were made estrous stage in this report.
in a FD-2A type fracturing device as previFreezeFracture
ously described (Toshimori and Oura, 1982).
The zonulae occludentes in mouse oviducLanthanum Infusion
tal epithelium resemble those of other epiA fixative containing 2.5% glutaraldehyde thelia in the general arrangement of their
and 2% lanthanum nitrate (pH 7.2 adjusted elements (more or less continuous bands
by 0.1 M cacodylate buffer) was infused made up of ridges on the P-face and grooves
through the thoracic aorta in two adult mice on the E-face). Ciliated cells are easily differ-
*
259
ZONULAE OCCLUDENTES IN MOUSE OVIDUCT
TABLE 1. Number
of
zonulae occludentes between adjacrnt cells at various regions’
8-C
Cell
Control oviduct
(diestrous)
Isthmus
(estrous)
Ampulla
(estrous)
1
I1
I
I1
I
I1
s-s
c-c
19
15
35
8
26
12
- ___
S
C
9
26
25
20
22
6
10
6
6
9
9
3
2
10
11
8
I
1
Total
40
60
69
31
61
33
100
100
100
‘S= secretory (nonciliated) cell (S-S = between adjacent secretory cellsi; C = ciliated cell (C-C = hetween adjacent
cillated cells); I = type I (parallel]zonula occludens; I1 = type I1 (anastornosing) zonula occludens.
entiated from secretory (nonciliated) cells by
the presence of the so-called “necklace” at
the ciliary base (Figs. 2, 3, 5) as reported by
Inoue and Hogg (1977) and Komatsu et al.
(1979).
The zonulae occludentes were classified
into two cases: 1) zonulae occludentes between adjacent secretory cells (Fig. 1)or between adjacent ciliated cells (Fig. 2) and 2)
zonulae occludentes between secretory and
ciliated cells (Fig. 3). Further, each zonula
occludens was classified into two types: parallel type (I) or anastomosing type (11). The
criteria for classification were as follows:
Type I zonula occludens had many strands
running parallel to the luminal surface,
whose branching points were very few (Figs.
4, 5). Type I1 zonula occludens had many
strands anastomosing frequently, whose
branching points were much greater in number than those of type I (Figs. 1-3). Abluminal strands in these junctions frequently
displayed terminal loops and/or free-ends
(Figs. 2-5) as reported by previous workers
(Pitelka et al., 1973; Staehelin, 1974; Tice et
al., 1975; Suzuki and Nagano, 1978). Such a
configuration was recognized as a new junctionai formation area (iunction assembiv or
extension) by previouslworkers (Tice et“ al.,
1975; Suzuki and Nagano, 1978).Further, in
this study, terminal loops and/or free-ends
were observed in both types of zonulae occludentes in both types of cells (Figs. 2-5).
Therefore, we determined a type of zonula
occludens, preferentially based on the structure in the adluminal strands, excluding the
abluminal strands with terminal loops-and/
or free-ends. Zonulae occludentes with a
structural nature of both types, which were
sometimes observed in various regions, were
ruled out for purposes of quantitation.
The number of type I or I1 zonulae
occludentes
The number of type I or I1 zonulae occludentes on each cell is presented in Table 1.
As to the numerical MI ratio in adjacent
secretory cells, the difference between the
control oviduct and the isthmus was statistically significant (P < .001), while the difference between the control oviduct and the
ampulla was not significant (.05 < P < .lo).
As to the numerical I/II ratio in adjacent
ciliated cells, the difference was statistically
significant (P < .001) in either case-the control oviduct versus the isthmus, and the control oviduct versus the ampulla. Such a
tendency was shown between secretory and
ciliated cells as well. As to the numerical I/II
ratio in total number, the difference between
diestrous stage and estrous stage was statistically significant (P < .001) in either casethe control oviduct versus the isthmus, and
the control oviduct versus the ampulla.
Therefore, the zonulae occludentes at diestrous stage were predominantly anastomosing, while those a t estrous stage were
predominantly parallel.
Junctional morpholom
-The number of strands and the depth occupied by junctional strands is presented in
Table 2. The lowest mean value of junctional
strands comprising the zonulae occludentes
was 5.3 f 1.6 in type I1 zonula occludens in
the ampulla. Comparing the diestrous stage
t o the estrous stage, no significant differA b breuiations
D
E
P
Desmosome
E-face
P-face
Figs. 1-3. Type I1 (anastornosing) zonulae occludentes
from the control oviduct (diestrous stage).
Fig. 1. Zonula occludens between secretory cells.
Grooves, which are registered with strands, anastomose
frequently on the E-face. The depth occupied by junctional strands is about 1 pm. A cluster of pits which
correspond to gap junctional particles is displayed on the
E-face (circles). x 47,000.
Fig. 2. Zonula occludens between ciliated cells. Ciliated cells are differentiated from secretory cells by the
presence of the so-called ciliary necklace (asterisks).Note
some abluminal strands show free-ends (arrowheads), A
rectangular-shape cluster of intramembraneous particles is demonstrated on the P-face (circle). A three-cell
junction is observed between double arrowheads.
x 39,000. Inset) High magnification of many rectangular-shape clusters of particles similar t o that in encircled
area of Fig. 2. x 90,000.
Fig. 3. Zonula occludens between secretory (S) and
ciliated (C) cells. Terminal loops (arrowheads) are seen.
Desmosomal patches are also seen. x 36,000.
Fig. 4. Type I parallel 'Onula occludens between secretory cells from the isthmus a t estrous stage. Grooves
run parallel to each other in the adluminal region (cornpare Fig. 4 to Figs. 1-3). Free-ends are seen (arrowheads). x 73,000.
Fig. 5 . Type I zonula occludens between ciliated cells
from the ampulla at estrous stage. Some abluminal
strands also show free-ends (arrowheads). x 33,000.
262
K. TOSHIMORI, R. HIGASHI, AND C. 6 U R A
+o m m
ences were seen in junctional morphology except for the number of strands of type I1
zonula occludens on secretory cells: the control oviduct versus the ampulla (P < .05).
Type I zonulae occludentes always had more
strands than those of type 11. Further, type I
zonulae occludentes had significantly more
strands on secretory cells than on ciliated
cells in each region-control oviduct, P < .01;
isthmus, P < .001; ampulla, P < ,005. Type
I1 zonulae occludentes had significantly more
strands in secretory cells than in ciliated cells
only in the control oviduct (P < .05). The
distance between adjacent strands (mainly
30-50 nm in the adluminal regions) was similar for all regions at both diestrous and estrous stages. The depth occupied by
junctional strands was a t least 0.51 & 0.20
pm in all zonulae occludentes. The depth was
likely to be deeper at diestrous stage than at
estrous stage. However, the minor differences in depth shown in Table 2 were not
statistically significant.
Maculae adherentes (desmosomes), which
were displayed as characteristic patches of
various-sized particles (Figs. 2, 3), were frequently observed below the occluding junctional domain in the epithelium at all regions
of the oviduct. Nexuses (gap junctions) were
rarely encountered in connection with the
strands of zonula occludens in this epithelium (Fig. 1). However, many rectangularshaped clusters of small intramembraneous
particles (diameter, about 60 A ) were sometimes observed below the occluding junctional domain or basalward in the epithelium
(Fig. 2).
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Lanthanum Infusion
The lanthanum nitrate infused into the
bloodstream permeated into the intercellular
spaces between the epithelial cells in all regions. The tracer usually permeated the occluding junctional domain to within a very
short distance from the luminal surface, and
it could reach toward the luminal surface
beyond the junctional domain in some regions (Fig. 6).
DISCUSSION
The present study demonstrates that the
zonulae occludentes between oviductal epithelial cells are different in their geometrical
structure between diestrous and estrous
stages in the mouse: The anastomosing type
is predominant a t the diestrous stage, and
the parallel type is predominant at the es-
ZONULAE OCCLUDENTES IN MOUSE OVIDUCT
263
Fig. 6 . Lanthanum infusion. The exogenous tracer
permeates into the intercellular spaces. The tracer appears to he stopped at the juxtaluminal region (arrows),
but it reaches toward the luminal surface in some regions (double arrows). X 7,400. Inset) High magnifica-
tion of another juxtaluminal region. The tracer reaches
toward the luminal surface beyond the occluding junctional domain (arrowhead). Some junctional elements
(arrows) are outlined by tracer in negative contrast. x
49,000.
trous stage. Since the reciprocal relationship
between estradiol and progesterone levels in
serum have been clearly elucidated during
the 4-day estrous cycle in the rat (Kalra and
Kalra, 19741, the progesterone dominant period is thought t o be coincident with the diestrous stage in this study, while the estrogendominant period is coincident with the estrous stage. Such a cyclic variation in morphology of zonulae occludentes is similarly
reported in the rat uterine endometrium by
Murphy et al. (1981). They stated that the
frequently interlocked tight junctions (with
many “t” intersections) were predominant
when progesterone was administered to
ovariectomized rats, while less frequently interlocked ones (with few “t” intersections)
were predominant when estrogen was adminstered. Since hormonal change affects not
only uterine endometrial epithelium but also
oviductal epithelium, it seems reasonable
that the present result is in accord with that
of Murphy et al. (1981). However, these data
do not correspond in all respects to those
reported by Komatsu et al. (1979),who stated
that the zonulae occludentes between secretory cells were anastomosing, while those between ciliated cells were parallel in mouse
oviduct. In our opinion, the structural type of
zonula occludens fluctuates according to the
ovarian hormone level in serum. Therefore,
we agree with the concept that tight junctional configurations are dynamically interchangeable (or reconstructable) under various conditions (Pitelka et al., 1973; Humbert
et al., 1976; Montesano et al., 1976; Suzuki
and Nagano, 1978).
The present data showing that the depth
occupied by junctional domain at the diestrous stage is likely to be deeper than that at
264
K. TOSHIMORI, R. HIGASHI, AND C. 6URA
the estrous stage make us agree with Murphy et al. (1981), who reported that the tight
junctions extended more deeply down in the
rat uterine endometrium when progesterone
was administered.
The zonulae occludentes between oviductal
epithelial cells are thought to be tight enough
morphologically to seal intercellular spaces,
since they belong to the category of tight type
according to a classification proposed by
Claude and Goodenough (1973). The sealing
effect of such zonulae occludentes is supposed
not to be seriously affected by ovarian hormones at any region in the mouse oviduct
throughout the estrous cycle.
On the other hand, the result of lanthanum
infusion suggests that the zonulae occludentes in the oviductal epithelium do not
always function as a diffusion barrier to the
exogenous tracer. Martinez-Palomo and Erlij
(1975) reported that the permeability of zonulae occludentes was not directly correlated
with the number of junctional strands. The
labeled proteins identical or similar to those
in serum were confirmed to be transferred
from the ampulla of the oviduct to the developing embryo, while reverse transfer from
the lumen to the oviductal epithelium did
not occur in mice (Glass, 1969). Such serum
type proteins are supposed to be due to a
combination of a transudate from bloodstream and an active secretion of secretory
cells (Mastroianni et al., 1970; Moghissi,
1970). Further, immunoglobulins have been
confirmed to be present in the human oviduct, and they are postulated to have a role
in immunologic infertility (Moghissi, 1970).
Lanthanum nitrate is currently considered
to be a “small” tracer in which it is impossible to evaluate the actual size and molecular
weight due to a charged molecule binding to
various substances in the intercellular space
(Tice et al., 1977). Therefore, an experimental probe using such exogeneous tracers as
horseradish peroxidase (moJecular weight,
40,000; diameter, about 50 A), microperoxidase (molecular weight, 1,900; diameter,
about 20 A), and 5-hydroxydopamine (molecular weight, 256, diameter, 5-7 A ) is necessary to assess the permeable molecular
weight through intercellular spaces a t various regions of the oviduct during the estrous
cycle. Further, the exogeneous tracers need
to be applied under physiological conditions.
Exogeneous tracers including lanthanum nitrate can alter its permeability among differ-
ent epithelia under various experimental
conditions (Brightman and Reese, 1969;
Goodenough and Revel, 1970; Friend and
Gilula, 1972; Machen et al., 1972; Wade et
al., 1973; Martinez-Palomo and Erlij, 1975).
Since lanthanum nitrate was applied along
with fixative in this study, its increased degree of penetration is not a reliable reflection
of permeability in the physiological state.
The zonulae occludentes are thought not only
to store the luminal fluid that provides a
medium for the passage of spermatozoa and
ovulated ova through the oviduct but also to
prevent the escape of spermatozoa and ovulated ova or their degradation products from
the lumen to the extracellular space (or to
the bloodstream), which would induce a n immune response (production of antibodies to
spermatozoa and autoantibodies to ova).
One could speculate from the number of
parallel- or anastomosing-type zonulae occludentes (Table 1)that secretory cells are more
effective barriers than ciliated cells in the
isthmus, while the reverse is true in the ampulla. It is of interest that this correlates
with the fact that secretory cells are more
numerous in the isthmus, while ciliated cells
are more numerous in the ampulla (Clyman,
1966; Hafez, 1973).
The patterns of occluding junctions are related to variations in the cell shape (Pitelka
et al., 1973; Hull and Staehelin, 1976; Suzuki
and Nagano, 1978). In the mouse oviduct,
secretory cells increase in height as they increase in secretory activity during the estrous stage (Beier, 1974).Further, Suzuki and
Tsutsumi (1981) reported in the normally
mated rabbit that intraluminal pressure of
the oviduct increased during estrous and then
declined gradually during the period of egg
transport through the isthmus. Therefore,
when the idea proposed by Hull and Staehelin (1976) is adapted to the present results,
the zonulae occludentes in the oviduct may
become flexible during estrous stage due to
increased stress from luminal contents and
cytoplasm under the influences of estrogen,
while they may become less flexible during
diestrous stage due to decreased stress after
resorption of luminal contents and cytoplasm
under the influence of progesterone,
It is also reasonable that adjacent epithelial cells are tightly conjoined by many maculae adherentes to endure the vigorous
movement of cilia throughout estrous cycle,
since maculae adherentes, which are well
ZONULAE OCCLUDENTES IN MOUSE OVIDUCT
known to serve as cell-to-cell adhesion (Farquhar and Palade, 1963; Friend and Gilula,
1972; Staehelin, 19741, are frequently observed in the oviductal epithelium. Further,
the occluding junctions are also implicated in
the adhesive function as well as providing a
permeability seal (Farquhar and Palade,
1963; Brightman and Reese, 1969; Pitelka et
al., 1973; Montesano et al., 1975; Pinto da
Silva and Kachar, 1982). However, it is still
unclear whether or not adjacent epithelial
cells are well coupled ionically or metabolically throughout the estrous cycle, since nexuses, which are well known as communicating junctions (Peracchia, 1980; Hertzberg et al., 1981), are sometimes, but not
frequently, discernible in the oviductal epithelium.
ACKNOWLEDGMENTS
The authors thank Dr. R.J. Adams for his
advice on English usage. This work was supported by Grants-Aid for Scientific Research
from the Ministry of Education, Science, and
Culture of Japan (No. 557009, No. 56770019,
No. 57770026).
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oviductal, quantitative, cells, mousefreeze, occuldentes, epithelium, stage, stud, estrous, diestrous, analysis, zonular, fractured
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