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Ultrastructural evidence that specialized regions of the murine oviduct contribute a glycoprotein to the extracellular matrix of mouse oocytes.

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THE ANATOMICAL RECORD 221~720-729(1988)
Ultrastructural Evidence That Specialized Regions
of the Murine Oviduct Contribute a Glycoprotein to
the Extracellular Matrix of Mouse Oocytes
RAJ P. KAPUR AND LINCOLN V. JOHNSON
Department of Anatomy and Cell Biology, University of Southern California, School of
Medicine, Los Angeles, California 90033
ABSTMCT
Previous studies have identified a glycoprotein (GP215) that is secreted by the murine oviductal epithelium and subsequently becomes sequestered
within the perivitelline space of oocytes and developing embryos (Kapur and Johnson,
Dev. Biol. 112:89-93, 1985; J. Exp. Zool. 238:249-260, 1986). The ultrastructural
localizations of GP215in the perivitelline space of ovulated oocytes and in the oviductal
epithelium are described here. The glycoprotein is shown to be associated with a
morphologically discrete extracellular matrix that provides a unique microenvironment for fertilization and early developmental events. In addition, putative secretory
granules that contain this glycoprotein are observed in specificsegments of the murine
oviductal epthelium, suggesting regional differences in the composition of oviductal
secretions.
The mammalian oviduct functions as more than a
simple tubular conduit for the movements of gametes
and embryos between ovary and uterus. The oviduct is
also a sophisticated secretory organ that maintains and
modulates a dynamic fluid-filled milieu in which maturation of gametes is completed, fertilization occurs,
and early embryonic development begins. Along its
length, the oviduct establishes regional and temporal
differences in the ionic (David et al., 1969; Borland et
al., 1977) and macromolecular (David et al., 1969; Mastroianni et al., 1970; Kay and Fiegelson, 1972; Noske
and Daniel, 1974) composition of oviductal fluid to accomodate these varied reproductive and developmental
events.
Physiological conditions in the oviductal lumen have
been shown to influence gamete interaction and embryonic development. This has been documented most
clearly in amphibian oocytes, which become fertilizable
after their interaction with proteinaceous oviductal secretions that associate with the vitelline envelope (Grey
et al., 1977; Miceli and Fernandez, 1982).The potential
importance of mammalian oviductal secretions in preparing egg or sperm for fertilization has not been demonstrated so clearly. Although the success of in vitro
fertilization of preovulatory oocytes (Schroeder and Eppig, 1984) has established that oviductal secretions are
not absolutely required in mice as in anurans, there is
evidence that factors produced by the oviduct significantly affect the frequency of mammalian fertilization
(Lambert and Hamner, 1975). In addition, several studies have demonstrated the existence of oviductal secretions that influence the success of early embryonic
development (Greenwald, 1962;Kille and Hamner, 1973;
Cline et al., 1977; Richardson et al., 1980; Van Winkle
et al., 1985).
Proteinaceous components of oviductal fluid, secreted
by the oviductal epithelium, are likely to be important
0 1988 ALAN
R. LISS, INC.
in influencing intraluminal events. Electrophoretic
studies have identified proteins (Marcus and Saravis,
1965; Mastroianni et al., 1970; Noske and Daniel, 1974;
Fazleabas and Verhage, 1986) and immunological studies have identified antigens (Glass and McClure, 1965;
Fox and Shivers, 1975a,b; Gaunt, 1985) that appear to
be secreted by the mammalian oviduct, but few of these
have been well characterized (Kay and Fiegelson, 1972;
Barr and Oliphant, 1981). In some instances, proteins
produced by the oviduct, have been shown to bind to
the surface of, or accumulate within, developing embryos (Greenwald, 1959; Glass, 1969; Fox and Shivers,
1975a,b; Gaunt, 1985).
Previously, we described a 215-kD glycoprotein
(GP215) that is secreted by murine oviductal epithelium and associates secondarily with ovulated oocytes
and cleavage-stage embryos (Kapur and Johnson, 1985,
1986). GP215 is present in oviductal epithelium and
ovarian bursa1 and oviductal fluids. The glycoprotein
becomes sequestered selectively in the perivitelline space
between the zona pellucida and the plasma membrane
ofthe oocyte/embryo and it remains concentrated in this
space until the zona pellucida is shed.
Electron microscopic immunolocalization of GP215 in
the perivitelline space of ovulated oocytes and in the
cytoplasm of oviductal epithelial cells are presented here.
Structural and immunological evidence is provided for
the existence of a distinct perivitelline microenvironment bounded by the zona pellucida. GP215 is a component of this unique microenvironment that occupies the
space immediately surrounding the oocyte or embryo. In
addition, ultrastructural observations of the murine oviduct are presented that reveal marked regional differ-
Received August 31, 1987; accepted December 22, 1987.
OVIDUCTAL PRODUCT IN PERIVITELLINE MATRIX
ences in the morphological and biochemical features of
its secretory epithelium.
METHODS
Collection of Murine Oviducts and Oocytes
Female ICR mice, 6-8 weeks old, were superovulated
in synchrony by successive intraperitoneal injections of
5 IU of pregnant mare’s serum gonadotropin (Teikoku
Mfg. Co., Tokyo) followed 44-48 hr later with 5 IU of
human chorionic gonadotropin (HCG, Calbiochem, La
Jolla, CA). At 16-24 hr after HCG injection, oviducts
from superovulated mice were excised and immersed
immediately in either fixative (see below) or 0.01 M
phosphate-buffered saline (PBS, pH 7.4). Postovulatory
ova were liberated from oviducts in PBS by tearing the
wall of the dilated ampulla with forceps. Cumulus cells
were removed with hyaluronidase as described previously (Kapur and Johnson, 1986).
Fixation and Embedding of Oviducts and Oocytes
Oviducts and oocytes were fixed by immersion for
3-4 hr in 0.1 M sodium cacodylate buffer containing
either 4% paraformaldehyde or 2% paraformaldehydel
2% glutaraldehyde and then rinsed several times in
cacodylate buffer.
Oviducts were rinsed overnight in two changes of
cacodylate buffer and cut into infundibular, ampullary
and isthmic segments. Oviductal segments were
embedded in Lowicryl according to the procedure of
Altman et al. (1983). Briefly, the tissues were dehydrated through a graded series of dimethylformamide
(DMF) solutions, and subsequently infiltrated with
Lowicryl K4M embedding medium (Polysciences,Warrington, PA; 6 gm cross-linker, 39 gm monomer, 0.225
gm initiator). The tissues were transferred to gelatin
capsules containing embedding medium and placed in
the dark at -15°C for 15 min. Finally the resin was
polymerized by exposure to long-wavelength ultraviolet
light for 45-90 min; some soft blocks were hardened by
incubation at 60°C.
Oocytes were partially dehydrated in 50% dimethylformamide for 1 hr. Further dehydration was avoided
because it was observed to cause dissolution of the zona
pellucida. The oocytes were then infiltrated with pure
embedding medium, transferred to conical capsules filled
with embedding medium, and centrifuged for 2 min
(14,OOOg)t o pellet the oocytes. The embedding solution
was polymerized under ultraviolet light at - 15°C for
45-90 min.
Oviducts were fixed in one-half strength Karnovsky’s
fixative (2% paraformaldehyde, 2.5% glutaraldehyde,
0.1 M sodium cacodylate, and 0.025% calcium chloride,
pH 7.4) and postfixed for 2 hr in cacodylate buffer containing 1%OsO,. Entire oviducts or oviductal segments
were dehydrated by equilibration in a graded series of
ethanol solutions, followed by incubation in propylene
oxide.The dehydrated tissues were infiltrated with Epod
Araldite resin (30% Epon 812, 18%Araldite 502, 52%
dodecylsuccinic anhydride and 1.5% 2,4,6-trimethylaminomethvl Dhenol) and transferred to gelatin capsules filled kith EpodAraldite resin for polymerization.
721
lmmunolabeling of Intact Oocytes and Tissue Sections
The preparation and specificity of the polyclonal antiGP215 antibody (A-GP215) and “nonimmune” immunoglobulin, and the procedures used to immunolabel
intact oocytes, have been detailed elsewhere (Kapur
and Johnson, 1986).
Semithick (1 Fm) and thin sections (100 nm) of oviducts and oocytes were cut on an ultramicrotome (MT2B, Sorvall Porter-Blum, Newton, CT) with a glass knife
and collected on glass slides or uncoated nickel grids
(300 mesh, Ted Pella Inc., Tustin, CA), respectively.
For immunofluorescence assays, semithick sections of
murine oocytes were labeled by incubation for 30 min
in A-GP215 diluted 1:20 with PBS containing 1mM
MgCl,, 1 mMCaCl,, and 0.5% BSA (PBSMC-BSA).
After two 15 min rinses with PBSMC-BSA, fluorescein-conjugated rat anti-chicken IgG (1:20 dilution; Kirkegaard and Perry Laboratories, Gaithersburg, MD) was
applied for 30 min. The sections were rinsed, mounted,
observed, and photographed as described previously
(Kapur and Johnson, 1986).
Thin sections of oocytes or oviductal tissue were rinsed
for 5 min with PBSMC-BSA and then incubated for 1
hr in A-GP215 diluted 1:lOO with PBSMC-BSA. After
two rinses of 15 min each, the sections were incubated
in biotinylated goat anti-chicken antiserum (Kirkegaard and Perry Laboratories, Gaithersburg, MD) diluted 1:20; rinsed again, and incubated 1hr in colloidal
gold-conjugated avidin diluted 1:20 (20 nm gold particles; Janssen Pharmaceutica, Beerse, Belgium). Finally
the sections were rinsed three times for 10 min with
PBSMC-BSA followed by a brief rinse with distilled
water.
In all the electron microscopic experiments described,
the sections were stained after immunolabeling with
2.5% uranyl acetate (5 min) and Reynold’s lead stain
(5-10 sec) (Reynolds, 1963). EpodAraldite-embedded
tissues were stained with the two reagents for 10 min
and 5 min, respectively. The sections were observed and
photographed with a JEOL-100C electron microscope.
An effort was made to photograph fields that represented the typical features of all the tissues labeled in
the same manner. In all cases, control tissues were
prepared by substituting equivalent amounts of “nonimmune” immunoglobulin for A-GP215.
RESULTS
Localization of GP215 in Association With Oviductal Oocytes
Immunofluorescence localization of GP215 in association with living oocytes still surrounded by cumulus
cells demonstrates that the glycoprotein is selectively
sequestered within the perivitelline space, but is not
detected in the cumulus matrix (Fig. l a , b). In addition,
GP215 is not present within the cytoplasm of the oocyte
in an immunologically recognizable form (Fig. lc,d).
Electron microscope observations of immunolabeled
postovulatory oocytes confirm sequestration of GP215
in the perivitelline space. At the ultrastructural level,
the perivitelline space of postovulatory oocytes contains
a meshwork of flocculent material and particles. Virtually all of the binding of A-GP215 to sections of postovulatory oocytes is localized to this perivitelline matrix
(PVM). Immunolabeling is seen throughout the perivitelline space from the surface of the oo&e to the inner
722
R.P. KAPUR AND L.V. JOHNSON
Fig. 1. A washed oviductal oocyte with associated cumulus cells (b)
has been compressed to show, by immunofluorescence,A-GP215 binding
to substances within the perivitelline space (pvs). No specific fluorescence
is associated with the zona pellucida (z), vitellus (v), cumulus cells, or
A Nomarski differential interference contrast micumulus matrix (cm).
crograph of the same oocyte is presented for comparison (a). Immuno-
fluorescence l a b e h g of A-GP215 bindmg to a 1-pm section of an oviductal
oocyte (d)shows immunoreactivityin the perivitelline space, but neither
in the vitellus cytoplasm (V) nor in the zona pellucida (Z). A phasecontrast micrograph of an adjacent section is shown for comparison (c).
Bar: a,b, 50cm; c,d, 20pm.
surface of the zona pellucida, except where there are
gaps in the PVM (Fig. 2). The zona pellucida and oocyte
cytoplasm of A-GP215-treated sections (Fig. 2) and the
perivitelline space of control sections are not labeled
above background levels (Fig. 3).
The PVM has a looser and less ordered appearance
than the mesh-like zona pellucida so that the two
matrices are easily distinguished. The PVM appears to
be composed of at least two morphologically distinct
components (Fig. 2b). The first appears as clouds of
amorphous, lightly stained material (Fig. 2b, labeled
c). A particulate component of the PVM is observed
within or a t the periphery of these clouds (Fig. 2b, ar-
rowheads).The colloidal gold particles that identify areas
of GP215 immunolocalization are often clustered into
groups of three or four and seem to be associated with
the more amorphous material.
Localization of GP215 in Oviducts! Epithelium
Ultrastructural immunolocalization shows A-GP215
to bind heavily and selectively to putative secretory
granules in the apical cytoplasm of nonciliated oviductal epithelial cells (Figs.4b, 5). Areas within these cells,
identified as Golgi and endoplasmic reticulum, also appear to be labeled (Fig. 4b). Higher magnification shows
antibody binding to be most concentrated in association
Fig. 2. Transmission electron micrograph of a sectioned oocyte &r
immunolabeling with A-GP215 (a). Numerous gold particles (e.g. arrows), indicative of A-GP215 binding, are scattered throughout the perivitelline space. Labeling is associated with an extensive perivitelline
matrix that fdls the space between the zona pellucida and the surface
ofthe vitellus. The principal ultrastructural features of the perivitelline
matrix are shown more clearly at higher ma&ication (b) to consist of
cloudy materids of variable density (c) and electron-dense particulate
matter (arrowheads),which is o&n associated with the amorphous clouds.
Most of the A-GP215 immunolabeling in the perivitelline matrix is associated with the cloud-like material rather than the dense particles.
Bar: a, lpm; b, 0.5pm.
724
R.P. KAPUR AND L.V. JOHNSON
OVIDUCTAL PRODUCT IN PERIVITELLINE MATRIX
Fig. 5. "Ins micrograph shows an oblique section through the ampullary epithelium near the tip of a villous process. Portions of three
nonciliated epithelial cells (N,, NP,N,) and one ciliated cell (C) are
shown. Gold particles (arrows) indicate A-GP215 binding sites. GP215
is localized almost exlusively in the adluminal cytoplasm of nonciliated
725
epithelial cells. Most of the activity is associated with flocculent, electron-dense material in spaces likely to represent secretory vesicles. A
higher magnification ofthis labeling is shown in the inset (lower right).
L, lumen. Bar: l p m ; Inset, 0.5 pm.
orescence studies (Kapur and Johnson, 1986), populations of nonciliated cells that lack putative secretory
granules (Fig. 4a, central cell) and are not labeled by
A-GP215 exist in the oviductal ampulla and infundibulum (data not shown). In contrast to the oviductal
ampulla and infundibulum, no specific immunolabeling
was observed in the oviductal isthmus, although nonciliated cells containing secretory granules are present
(Fig. 7). However, the granules in the epithelium of the
isthmus are morphologically distinct from those in the
ampulla. In tissue sections prepared for immunolabelFig. 3.This electron micrograph shows a section of the same myte ing, characteristically either the isthmic granules are
as shown in Figure 2 &r labeling with nonimmune Ig, instead of A- devoid of electron-dense material or they contain a cenGP215, as a control for antibody specificity.Very few gold particles (e.g.,
tral electron-dense mass.
arrows) are observed in such control sections. Bar: 1pm.
Unlabeled sections of mouse oviductal infundibulum
Fig. 4. Electron micrographs of oviductal infundibular tissue observed and isthmus that have been fixed and embedded to
&r conventional preparation (a)and after immunolabeling with AGP215 6).
Immunoreactivityis localized almost entirely within putative better preserve epithelial cell morphology are presented
secretory granules (arrowheads in b) in the apical cytoplasms of non- for comparison (Figs.4a, 8). Densely stained granules
ciliated epithelial cells. These GP215-rich granules correspond to the are found in the cytoplasm of nonciliated cells of the
dense membrane-bound granules (arrows in a). Antibody labeling is also infundibulum (Fig. 4a) and ampulla (Fig. 8a,c) in an
concentrated in more basal cisternae (c), which probably represent endoplasmic reticulum and/or Golgi apparati. N, nucleus; L, lipid droplet. intracellular position and oviductal distribution similar
with flocculent material surrounded by vacuous electron-lucent areas that appear to represent disrupted
membranous vesicles (Fig. 5). Since control sections are
not labeled (Fig. 6), these flocculent areas presumably
contain GP215.
GP215 was detected only in a subpopulation of the
nonciliated epithelial cells of the oviductal ampulla and
infundibulum. As predicted from earlier immunoflu-
Bar: a,b, 2pm.
726
R.P. KAPUR AND L.V. JOHNSON
Fig. 6. A section of oviductal, infundibular epithelium that has been
labeled with nonimmune lg instead ofA-GP215 shows almost no binding.
A few scattered gold particles (arrows) are observed; but, in contrast to
A-BP215, virtually no labeling is associated with putative secretory vesicles (v) in the apical cytoplasm of nonciliated cells. C, ciliated cells. NC,
nonciliated cells. Bar: 1 pm.
t o the vesicular areas recognized by the A-GP215 antibody (Figs. 4b, 5). These cells are scattered throughout
the oviductal infundibulum and ampulla, where their
apical cytoplasms often project above the surfaces of
neighboring ciliated cells. A morphologically distinct
nonciliated cell type is found to constitute the majority
of the epithelial lining of the oviductal isthmus (Fig.
8b). In contrast to the ampullary and infundibular segments of the oviductal epithelium, numerous irregular
interdigitations exist between the lateral plasma memFig. 7. A section of oviductal isthmic epithelium that has been labeled
branes of isthmic epithelial cells. These cells lack the with A-GP215 shows no specfic labeling. Some gold particles that appear
be nonspecifically associated with the section are observed (thin arelectron-dense granules observed in the cranial oviduct. to
rows). Poorly preserved portions of cytoplasm under the apical plasma
Instead, they contain a population of apical granules membrane of many isthmic epithelial cells probably represent disrupted
with more diffuse and filamentous contents (Fig. 8d). secretorygranules (v).Some of these areas contain central electron-dense
masses (thick arrows) which are not bound by A-GP215. Bar: 0.5 bm.
DISCUSSION
The ultrastructural observations presented here further support our earlier suggestion that the murine
oocyte is fertilized and develops in a unique perivitelline microenvironment (Kapur and Johnson, 1986). This
microenvironment exists within the confines of the zona
pellucida and is biochemically and morphologically distinct from the greater fluid environments in which the
ovum or embryo resides. GP215 is a glycoprotein secreted by the oviductal epithelium that is selectively
concentrated as a component of this perivitelline microenvironment.
In the perivitelline space of postovulatory ova, GP215
appears ultrastructurally to be associated with a perivitelline matrix (PVM). This matrix fills the perivitelline space and immunolabeled GP215 is similarly
distributed, a finding that is in agreement with previous immunofluorescence analyses (Kapur and Johnson, 1986). The PVM has a reticular appearance despite
the fact that perivitelline GP215 has been shown to be
soluble in aqueous media (Kapur and Johnson, 1986).
However, the electron microscope image of this matrix
is likely to have been altered from its in situ state by
the fixation, dehydration, and embedding precedures.
Ultrastructurally, the murine perivitelline matrix
contains reticular and semiparticulate components,
similar to that described for pig and opossum PVM
(Talbot and DiCarlantonio, 1984a,b). However, neither
the opposum nor pig PVM contain the cloudy material
with which GP215 appears to be associated in the mouse;
it may be unique to murine oocytes. Although we do
not have data regarding GP215 secretion by opossum
or pig oviducts, GP215 is not detected in rabbit, guinea
pig, frog, or rat oviducts by immunofluorescence (Kapur, unpublished observations). Talbot (1985) also failed
to observe a PVM in mouse or hamster oocytes.
The binding of A-GP215 to putative secretory granules in nonciliated cells of the ampullary and infundibular segments of the murine oviduct agrees with earlier
OVIDUCTAL PRODUCT IN PERIVITELLINE MATRIX
Fig. 8. Ampullary (a,c) and isthmic (b,d) epithelial cells from the same
oviduct that have been fuced and embedded by conventional methods to
demonstrate the ultrastructural differences between the two regions.
Both ciliated (C) and nonciliated (NC) cells are observed in the ampulla;
in contrast, only nonciliated cells are observed in the isthmus. All the
cell types have long, branched microvilli (short arrows) on their apical
727
surfaces. Electron-dense granules (dg in c; white arrowheads in a) are
observed in the apical epithelium of nonciliated cells in the ampulla.
The morphologies of these contrast with the “mucinous”appearances of
granules (mg in d white arrowhead in b) seen in the oviductal isthmus.
Id, lipid droplet; n, nucleus; L, lumen. Bar: a,b 2.0 pm; c,d 0.5 km.
728
R.P. KAPUR AND L.V. JOHNSON
immunofluorescenceobservations (Kapur and Johnson,
1986). The fact that GP215 is localized only in the cranial segments of the oviduct indicates that the infundibular and ampullary epithelium is biochemically
distinct from that in the isthmus. This hypothesis is
supported by the observation that murine isthmic epithelial cells contain presumptive secretory granules that
are morphologically different from those in the ampulla
and infundibulum. Other studies of mammalian oviducts have indicated that the isthmus is morphologically (Nilson and Reinus, 1969), biochemically (Deane,
1952; Moog and Wenger, 1952; Zachariae, 1958; Lee et
al., 1983; Wu et al., 1983), and physiologically (Glass
and McClure, 1965; David et al., 1969) different from
the rest of the oviduct. A recent ultrastructural study
ofthe rabbit oviduct demonstrated that, as in the murine
oviduct, nonciliated cells in the ampulla and infundibulum contain electron-dense secretory granules, in
contrast to nonciliated cells in the isthmus, which contain electron-lucent “mucinous” granules (Jansen and
Bajpal, 1982). Although the functional significance of
such regional differences is not understood, they probably relate to the variety of developmental and reproductive events that occur along the length of the oviduct.
It seems reasonable that sperm migration, embryo
transport and differentiation, and other events hosted
by the oviductal isthmus may benefit from epithelial
secretions different from those important t o events that
occur in the infundibulum and ampulla, such as oocyte
maturation, cumulus cell dispersal, and fertilization.
The observations presented in this paper strengthen
the hypothesis that GP215 is secreted by the murine
oviduct and is sequestered subsequently in the perivitelline space. There are several reports of proteins, distinct from GP215, that are secreted by mammalian
oviducts, some of which become associated with the ovum
andor embryo (discussed in Kapur and Johnson, 1986).
In addition, Gaunt (1985) has described an antigen that
is recognized by a monoclonal antibody (NB5)that binds
to the surfaces of murine vitelluses, embryos, and teratocarcinoma cells, and, on the day of ovulation, to oviductal epithelium. NB5-antigen is initially acquired by
the ovum from the oviductal fluid; however, subsequently, the embryo becomes capable of synthesizing it.
Although pharmacological experiments suggest that
NB5-antigen is a glycoprotein, it is probably not GP215
for several reasons. The NB5 antibody binds to many
tissues, including uterus, that are not labeled by AGP215 (Kapur and Johnson, 1986).Unlike GP215, NB5antigen is associated with the surface of the vitellus
and is not lost after removal of the zona pellucida. In
addition, the temporal patterns of association of NB5antigen with the ovum, embryo, and oviduct are different from GP215. Therefore, NB5-antigen and GP215
are probably two different examples of glycoproteins
produced by the murine oviductal epithelium that associate with the ovum.
The developmental significance of macromolecules
passively acquired by postovulatory oviductal ova is not
established. However, specific localization of GP215 in
the murine oviduct and perivitelline matrix provides
further evidence that secretory products from the mammalian oviduct contribute to the formation of a specialized environment in which fertilization and important
early developmental events take place.
ACKNOWLEDGMENTS
The authors gratefully acknowledge valuable discussions with Dr. Richard Wood and Dr. Gregory Hageman. In addition, the clerical assistance of Mrs. Lynette
Kapur has been greatly appreciated. The studies described here were supported by grants from the National Institutes of Health (HD 15325) and the March
of Dimes Birth Defects Foundation (5-368, 1-97). LVJ
is the recipient of a Research Career Development Award
from the National Institute of Child Health and Human
Development.
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ultrastructure, contributes, matrix, specialized, oocytes, extracellular, murine, evidence, oviduct, mouse, glycoprotein, regions
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