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The ultrastructure of follicle cells in fetal guinea-pig ovaries.

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The Ultrastructure of Follicle Cells in Fetal
Guinea-pig Ovaries
Institute ofdnatomy, B, Uniuersity ofAarhus, DK-8OOAarhus C, Denmark
The development of the follicle cells in fetal guinea-pig ovaries
has been examined in the electron microscope.
The findings were as follows: a t days 34 and 38 there were broad intercellular
clefts within the germinal cords. However, a continuous layer of thin cytoplasmic processes from the follicle cells separated the germinal cords from the
stromal compartment. The germinal cords were everywhere limited by a basal
lamina. During all the period examined coated vesicles, possibly emptying their
contents into the region of the basal lamina, were observed in the follicle cells.
At days 42,46and 50 the cellular membranes were closely apposed with an intercellular distance of about 200 A. Complexes of deeply interdigitating folds of
the membranes of neighboring follicle cells were observed. The follicle cells forming part of the primordial follicles a t days 54 and 58 were characterized by a disappearance of these folds and by the appearance of bundles of microfilaments in
the cytoplasm. These were especially numerous a t day 66.
At days 34 and 38 gap junctions were observed between the follicle cells, but
not between the follicle cells and the germinal cells. During the entire period examined junctions resembling desmosomes without filaments were observed between the follicle cells as well as between the follicle cells and the germinal cells.
The ultrastructure of the follicle cells is considered in detail and the functional significance of the findings discussed.
From light microscopic studies of fetal ovaries of mammals it was generally concluded
that the follicle cells originated from the surface epithelium in a first and second proliferation under the formation of germinal cords
(Allen, '04;Bookhout, '46;Brambell, '27;Gillman '48;Weakley, '66;de Winiwarter, '01,
'10).However, Witschi ('51)claimed that the
follicle cells originated from a central blastema, and histochemical studies were interpreted in favor of this conclusion (Gropp
and Ohno, '66; Pinkerton et al., '61).Peters
and Pedersen ('67)suggested that the follicle
cells derived from central stromal cells.
Some electron microscopic examinations
have been carried out on fetal mammalian gonads (Gondos, '69, '70a,b; Gondos et al., '71;
Gondos and Zamboni, '69;Gonzalez-Angulo et
al., '71;Odor and Blandau, '69;Weakley, '67),
but only for part of the organogenesis, mainly
from the time shortly before birth. The aim of
ANAT. REC., 189: 649-668.
the present examination was to study the general changes in ultrastructure in follicle cells
during the morphogenesis of the guinea-pig
ovary from the time of early sexual differentiation a t day 34 until completion of organogenesis at day 66 (Bookhout, '45).Special interest
was focused on the development of cell components of presumed functional importance,
such as cell contacts and cytoplasmic microfilaments.
Twenty-three fetuses from a total of 14
albino guinea-pig mothers were examined a t
the following gestational days: 34,38,42,46,
50,54,58 and 66.A t least two fetuses of each
stage were studied.
The gestational age was calculated from the
day sperm were demonstrated in vaginal
smears within 24 hours after parturition (as
Received Mar. 7, '77. Accepted May 31, '77.
guinea pigs mate shortly after they have
delivered). The crown-rump length of each
fetus was measured and found to correspond
to the findings of Draper ('20).
Pregnant guinea-pigs were anesthetized
and cesarean section performed. With the umbilical cord still intact the thoracic cavity of
the fetus was opened and perfusion fixation
performed transcardially with the needle
placed in the left ventricle, the right atrium
being opened. Two percent glutaraldehyde in
cacodylate buffer (Sabatini et al., '63)with 2%
dextran T40 added (Bohman and Maunsbach,
'70) was used for perfusion (pH 7). The temperature of the fixative was 2-4"C, perfusion
pressure 100 mm Hg and the perfusion time
three minutes. Then the ovaries were immersed in the same fixative and a t the same
temperature for a t least three hours. During
this time the ovaries were cut under a dissection microscope. They were first cut longitudinally into two halves and then each half
was cut transversely into four or five slices.
They were subsequently post-fixed in 1%
osmium tetroxide in veronal acetate buffer
(pH 7.2-7.4) (Sjostrand, '67).They were then
en block-stained (Kellenberger et al., '58) for
one hour in 0.5% uranyl acetate in the same
buffer (pH 5.9)dehydrated in alcohol and propylene oxide or acetone and embedded in Epon
or Vestopal. One-micron sections were stained
with 1%toluidine blue and examined with the
light microscope for selection of suitable
areas. After trimming, thin sections with
silver interference colors were cut on an
L.K.B.microtome, stained with lead citrate
(Reynolds, '63) and examined in a Siemens
Elmiskop 1a.
germinal cells (arrows) and follicle cells (FC).
The cells in the germinal cords are tightly
packed, contrasting to the loosely arranged
cells in the stromal compartment (S).
Cellular communications connect the surface epithelium and the germinal cords without intervening stroma (CC). The germinal
cords and the stromal compartment are everywhere sharply demarcated from each other.
Day 34
At the earliest point in time examined the
germinal cords could be clearly distinguished
from the stroma, as they were surrounded by a
continuous basal lamina (fig. 2). This consisted of a homogenous, about 100-300 A thick,
more electron-dense zone, together with an
outer, looser zone of fibrillar material of 200500 A in thickness. The basal lamina was discontinuous in many places due to the fact that
there were connections between the germinal
cords and between these and the surface epithelium. Consequently, the limits of the germinal cords were difficult to determine in the
area immediately beneath the surface epithelium.
The cells immediately beneath the surface
epithelium were more tightly packed than
further down in the cortex, where there were
big intercellular clefts between the follicle
cells and between these and the germinal
cells. The latter occurred singly or in small
groups, incompletely separated by cytoplasmic processes from the follicle cells (fig. 2).
The contour of the follicle cells was very
irregular with numerous rather short cellular
processes (ca. 0.1 p). The nucleus was somewhat eccentrically located away from the
basal lamina. The cytoplasm formed long (up
to 5-6 p ) and thin (0.1-0.2 p ) cytoplasmic
As an introduction to the description of processes, lying in close proximity to the
the electron microscopic findings a survey is basal lamina. The cytoplasmic processes from
given, referring to a light microscopic picture neighboring follicle cells were closely apposed
of the guinea-pig ovary a t day 38 (fig. 1). The to one another, separated by a distance of
picture presents the elements of the ovary about 200 A,and formed a continuous cellular
that are mentioned in the electron microscop- layer between the basal lamina and the geric description.
minal cells (fig. 2). Only very occasionally was
Figure 1 shows the ovary covered with the a germinal cell observed that directly consurface epithelium, SE, consisting of a super- tacted the basal lamina. Further, the follicle
ficial layer of flattened to cuboidal cells under cells sent long thin cytoplasmic processes in
which are seen one to three layers of rela- between the germinal cells, separating them
tively tightly packed cells, mixed with ger- from one another (fig. 2).
The nuclei of the follicle cells were ovoid
minal cells.
The main part of the ovarian cortex consists and contained finely dispersed chromatin
of branching germinal cords (GC) containing with a few peripherally located lumps of het-
erochromatin. In most cells a peripherally
located nucleolus was seen.
The number of mitochondria averaged 1520/cell. Their shape was oblong and their
lengths ranged from 0.2-1.5 micron although
a few considerably longer mitochondria were
A sparse amount of rough-surfaced endoplasmic reticulum was seen. The cisternae
were slightly dilated, containing finely granulated material.
Smooth endoplasmic reticulum or lipid-like
inclusions were not seen.
Golgi regions were only seen in a few of the
cell profiles. Golgi vesicles were observed (fig.
4), with a diameter of 400-600A. At higher
magnification they were coated and contained
no stainable material. Vesicles with a similar
ultrastructure occasionally were seen close to
the cell membrane. In addition coated invaginations of the cell membrane were also seen
(fig. 4, inset), representing either secretion or
Cell inclusions, limited by a single membrane and containing finely granulated matrix were occasionally seen.
The cytoplasm was rich in ribosomes, partly arranged in small rosettes, but mainly lying freely and evenly distributed. A sparse
amount of fine microfilaments, distributed a t
random, and a few scattered microtubules
were also observed.
The cell surface
The follicle cells were loosely arranged and
exhibited cytoplasmic processes. Many of
these were relatively short and thick, but between the germinal cells and towards the
basal lamina they were up to 5 micron long
and averaged 1,000 A in thickness. In most
sections the processes were well separated
from the germinal cells, but in places close apposition occurred along sections ranging from
1,000-3,000 A in length. A t these places the
intermembranous distance was 100-200h.
Desmosome-like junctions between follicle
cells and germinal cells (figs. 3, 41, characterized by an intermembranous electron translucent zone about 100 A thick and a corresponding electron-dense zone of about the
same thickness on the cytoplasmic side of the
follicle cell and the germinal cell were common. The desmosome-like junctions were
65 1
often present between cytoplasmic processes
from the germinal cells and the follicle cells.
Microfilaments were not concentrated around
these junctions.
Other follicle cell processes ran closely apposed to similar processes from neighboring
follicle cells with an intermembranous distance of 100-200 A (fig. 2). Desmosome-like
junctions of the same appearance as those between the germinal cells and the follicle cells
were common in these regions.
In addition, gap junctions (figs. 3, 4) were
occasionally seen between the closely apposed
processes of neighboring follicle cells. When
present they were located in between two desmosome-like junctions. The length of the gap
junction in a single section varied between 0.2
and 0.5 micron. The membranes were very
closely apposed, but a narrow gap of about 20
A could be recognized in suitably thin sections
(fig. 3). Mitoses were very rarely observed.
Day 38
At this stage the compact part of the basal
lamina surrounding the germinal cords had
increased in thickness to about 600 A. Otherwise there were no changes from the appearance at day 34.
Days 42, 46 and 50
At day 42 numerous and broad connections
between the surface epithelium and the germinal cords were observed, but a t day 46 the
connections were not so numerous and more
slender (fig. 5).
The follicle cells were closely apposed everywhere and intercellular clefts were absent.
Many of the cells had a branched appearance
with long (up to 5 micron) and thin (300-400
A) cytoplasmic processes (figs. 6, 7). The nuclei were unchanged in appearance.
A varying number of mitochondria were
seen. A noted change a t day 50 was that a
majority of the mitochondria were spherical
in shape. Most cells contained rough-surfaced
endoplasmic reticulum, and in about half of
the cell profiles Golgi regions were seen. In
these cells, especially in the Golgi region, a
great number of coated vesicles occurred.
No smooth endoplasmic reticulum or lipidlike inclusions were seen.
The cell membranes were now everywhere
closely apposed with an intercellular distance
between both cell types of 180-300 A (fig. 7).
Between the germinal cells cytoplasmic proc-
esses from the follicle cells still occurred and
frequently one or more long (up to 5-6p ) and
thin (300-600A) processes were seen either a s
a wedge between or surrounding the germinal
cells (fig. 6). Such processes could often be
seen to originate from neighboring follicle
cells (fig. 7). The processes either ran parallel
for a considerable distance (up to several p) or
formed deep (about 1 p ) and up to 5 or more
interdigitating folds (fig. 7). Desmosome-like
junctions of the same appearance as those a t
day 34 were observed and very occasionally a
gap junction was seen between two follicle
cells, but never between the follicle cells and
the germinal cells. Coated vesicles were observed in the follicle cells, but only in the region of the basal lamina. During this period
the thickness of the basal lamina increased so
that by day 50 the thickness of the electrondense layer was 600-800 A and that of the
looser fibrillar layer was 1,000-2,000
From day 42 and onwards no mitoses were
found among the follicle cells.
Day 54
The surface epithelium now consisted of
mainly one layer of cells (the superficial cells)
which were largely columnar. The subepithelial cells had largely disappeared.
Formation of follicles had begun in the
deepest part of the cortex, next to the medulla, with single oocytes completely surrounded
by one layer of flattened follicle cells (fig. 8).
In the more superficial parts of the cortex
nests of germinal cells still occurred, incompletely separated by thin cytoplasmic
processes from the follicle cells.
There was a distinct difference between the
ultrastructure of the follicle cells in the superficial part and those in the deeper parts of
the cortex that formed part of the primordial
follicles. In the superficial part they resembled in every respect the follicle cells seen
a t day 50.
In contrast, the follicle cells that formed
part of the primordial follicles were larger,
the largest in a single section measuring
about 23 X 3 p and, being sickle-shaped, they
surrounded up to about one-third of the circumference of the oocyte. The nuclei as a rule
were also sickle-shaped. The number of mitochondria averaged 30 in one section in contrast to 10 to 15 in the superficial cells and
they were mainly spherical. In about half of
the cells bundles of parallel microfilaments
were seen (fig. 9).
No lipid inclusions or smooth endoplasmic
reticulum was observed.
In places, a space up to 1,600-1,800A wide
had formed between the oocytes and the follicle cells (fig. 9). In these spaces cytoplasmic
processes from the oocytes were seen embedded in a fine granular material. This was the
first stage in the formation of the zona pellucida. The interdigitating folds of processes
from neighboring follicle cells had almost
completely disappeared. There were many
desmosome-like junctions, especially between
the oocytes and the follicle cells. Gap junctions between follicle cells were only very
rarely found on this day and onwards.
Day 58
In the superficial layer, beneath the surface
epithelium, germinal cells still occurred in
nests, incompletely separated by the follicle
cells, but deeper in the cortex many more follicles had formed.
There were no significant changes in the ultrastructure of follicle cells from day 54: In a
few of the superficial cells microfilament bundles were observed.
The ultrastructure of the follicle cells from
the primordial follicles were unchanged from
that of day 54.
Day 66
The appearance of the follicle cells was
mainly unchanged from that a t day 58,with
two exceptions: (1) There were many more
bundles of microfilaments. Practically every
cell exhibited several bundles of 60-90 A microfilaments, with as many as about 20 filaments in each bundle (Fig. 11).The longest
bundles had a length of about 1 p and their
orientation was variable with respect to the
long axis of the cell. Apparently they had no
constant relation to any specific structure in
the cell; however, they were often seen lying
near by the mitochondria. At places the bundles seemed to contact the cytoplasmic membrane, but no signs of contractile activity (microvillous projections or retractions of the cy.
toplasmic membrane) were observed (fig. 10).
(2) The beginning of zona pellucida formation was taking place along the entire circum
ference of the oocyte. Most of the cytoplasmic
processes seen in the zona pellucida originated from the oocyte, but a few could be identified as originating from the follicle cells. For
the first time coated invaginations of the cell
membrane of the follicle cells in the region of
the zona pellucida were observed, indicating
either secretion or endocytosis.
The thickness of the inner homogenous
layer of the basal lamina of the germinal cord
was unchanged (about 700 while the thickness of the fibrillar layer was about 2,000 A.
As regards the nucleus and the organelles
the cells were unchanged from day 58. No
smooth endoplasmic reticulum and no lipid inclusions were observed.
Origin of germinal cords
The electron microscope observations presented here and in another report (Jeppesen,
’75) indicate that, except for the germ cells,
the germinal cords originate from the surface
epithelium in the guinea-pig: the cellular connections between the surface epithelium and
the germinal cords contain cells with a morphology that is identical to the morphology of
the cells in either location (Jeppesen, ’75).
There is no demarcation line between the germinal cords and the surface epithelium a t the
sites of these connections; they are surrounded by a basal lamina that is continuous
with the subepithelial basal lamina as well as
with the basal lamina that continuously surrounds the germinal cords, separating them
from the stromal compartment. The presence
of microfilaments within a presumed contractile function in the superficial cells of the surface epithelium described previously (Jeppesen, ’75) may play a n important role in the
formation of the germinal cords. Odor and
Blandeau (‘69) did not observe cell cords originating from the surface epithelium, but this
may be because their examination began a t a
later stage in morphogenesis.
From the finding of tubules belonging to
the rete ovarii communicating freely with
the germinal cords in the medullary region,
Byskov and Lintern-Moore (‘73)concluded
that the follicle cells originate from the rete
ovarii. Based on experimental evidence Byskov (’74) suggested that the rete cells are responsible for the initiation of meiosis. This
suggestion, which is based on convincing data,
is compatible with the findings presented
here, which indicates that the surface epithelium contributes to the formation of the germinal cords. Cells of many sources contribute
to the formation of the gonad: germ cells of
extragonadal origin, the coelomic epithelium
and the mesenchyme. Therefore, it would in
my opinion not be impossible that the follicle
cells are derived from two sources: the rete
ovarii and the surface epithelium. Both cell
types are epithelial of nature, are relatively
undifferentiated and are both derived from
the mesoderm.
The increase in cell tightness in the germinal cord from day 34 to day 50 is according
to the present observations not due to mitotic
proliferation, as very few mitoses were observed. Probably the increase in cellular
tightness is caused by addition of new follicle
cells from the surface epithelium via the connections between the surface epithelium and
the germinal cords leading to a passive packing of the cells within the germinal cords.
Follicle cell-germ cell contacts
The appearance a t days 42-50 is in keeping
with the observations done by Gondos in the
rabbit (‘69, ’70b) who found that the adjacent
cell membranes of granulosa cells and germ
cells were closely apposed and that numerous
interdigitating cytoplasmic projections be tween the granulosa cells were present. However, he also found extensions of granulosa
cells indenting deeply into the cytoplasm of
germ cells. This was not found in the present
study, perhaps because different stages were
Gonzalez-Angulo et al. (‘71, horse) Odor
and Blandau (‘69, mouse), and Weakley (’67,
golden hamster) made essentially the same
observations. Weakley observed projections
from the follicle cells, indenting the germ
cells deeply, while the other authors did not
make this observation.
The gap junctions observed between follicle
cells a t days 34 and 38 have the same appearance as those observed by Bjorkman (‘62) and
Merk et al. (‘73) in the granulosa cells of the
mature rat ovary. They are presumed to play
an important role in intercellular communication, as it has been demonstrated in salivary
gland cells by means of tracers that this type
of junction is freely permeable for molecules
of a molecular weight of a t least 500, and that
this type of junction renders intimate communication between cells possible with free
exchange of ions, nutrients, intermediary metabolites and regulatory molecules (Staehelin,
’74).The presence of such junctions between
the follicle cells seems to indicate that the
germinal cells are surrounded by cells which
are all in the same functional state. Gap junc-
tions are only very occasionally found after
the fiftieth day.
The structure of the desmosome-like junctions between follicle cells and germ cells resembles that of other desmosomes except that
they lack a concentration of tonofilaments associated with them (Staehelin, ’74).
The function of the desmosome-like junctions between the follicle cells and the germinal cells is presumably only to form points
of adhesion. They persist even when the zona
pellucida is separating the germinal cells
from the follicle cells, and cytoplasmic processes from the follicle cells to the germinal
cells are found in these places. This is in keeping with the observations of Anderson and
Beams (‘60) and Weakley (‘66) in the ovary of
sexually mature guinea-pigs and golden hamsters, respectively. They found that the follicle cells sent cytoplasmic processes into the
region of the zona pellucida where they contacted the oocytes’ cytoplasmic membrane by
means of desmosome-like structures.
Coated vesicles
The presence of coated vesicles in follicle
cells with Golgi regions indicates that proteinacious material is probably synthesized
and secreted. Coated invaginations of the cell
membrane in the region of the basal lamina
were evident throughout the period examined,
and at day 66 coated invaginations of the cell
membrane in the region of the zona pellucida
were evident, indicating that either secretion
or endocytosis is taking place. I t is probable
that the described invaginations indicate secretion, as they were exclusively found in cell
profiles containing Golgi regions and coated
vesicles, but it cannot be excluded that they
represent endocytosis.
The nature of the microfilaments and the
function of the bundles of microfilaments is
unclear, but a few things should be noted: the
bundles of microfilaments only appear when
the cells form part of the complete primordial
follicle and thus have reached a resting stage.
Signs of contractile activity have not been observed.
Possibly the bundles of microfilaments
have a mere supportive function, as do the
filaments in other epithelial cells (Fawcett,
’66).The filaments described here resemble
closely the ones described by Schuchner and
Stockert (‘7%) with their random orienta-
tion, their wavy course and their dimensions
of 60-80 A. Schuchner and Stockert found
these filaments in granulosa cells from adult
Signs of steroid synthesis (smooth-faced endoplasmic reticulum and lipid inclusions,
Fawcett, ’66) were not observed.
Follicle cell-germinal cell interaction
As regards cellular interaction between the
follicle cells and the germinal cells no signs of
endocytosis or secretion (except in the zona
pellucida region) have been found. No gap
junctions or intercellular bridges between the
follicle cells and the germinal cells have been
found. The most intimate relation observed
was the described desmosome-like junctions
where the intermembranous distance is unaltered (about 200 A). How the two types of
cells influence each other (which they presumably do, Zuckerman, ’62) and whether the
germinal cells receive nutrients through or
between the follicle cells remains unclear.
Glass and Cons (‘68) demonstrated by injecting radiolabeled foreign protein antigen intravenously in female mice that the injected proteins could be demonstrated in the follicle
cells and the oocytes of complete follicles two
hours after the injection. Moreover, Neaves
(‘72) in the lizard demonstrated by means of
tracers a n extracellular route between the follicle cells from the circulation to the oocyte.
The technical assistance of H. Halse, A.
Meier, Th. Nielsen and K. Wiedemann is
gratefully acknowledged.
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1 Fetal ovary a t day 38, light microscopy, showing t h e surface epithelium BE), the ger-
minal cords (GC) containing germinal cells (arrows) and follicle cells (FC).Further,
the cellular communications between the surface epithelium and the germinal cords
is shown (CC). The sharp demarcation between t h e germinal cords and the stromal
compartment (S)is demonstrated. X 300.
2 Fetal ovary a t day 34.Part of germinal cord, containing follicle cells (FC) and germinal cells (GC). There are big intercellular clefts. The long thin processes of the follicle cells are seen separating the germinal cells (arrows). Basal lamina (BL). X 5,000.
3 Fetal ovary a t day 34. Two types of junctions are shown. At the left (a) is shown a typical junction (J)between a germinal cell (GC) and a follicle cell process (FC) (see text). X 120,000. Figure a t right (b) shows a gap junction between two
follicle cells. Gap (G)is seen. X 20,000.
Th. Jeppesen
Fetal ovary a t day 34. Two follicle cells (FC)are seen with long and thin cytoplasmic
processes. One cell contains a Golgi region with associated vesicles (arrow). This cell
forms a desmosome-like junction (J) with the germinal cell (GC) and a gap junction
(GJ) is seen between two follicle cells. One follicle cell faces the basal lamina (BL).
x 11,000.
Inset: Coated invagination of the cell membrane. Basal lamina (BL). X 42,750.
Th. Jeppesen
5 Connection between the surface epithelium (SE)and a germinal cord (GC)(day 46).
The connection is slender. x 2,890.
Th. Jeppesen
66 1
6 Fetal ovary at day 46. Part of germinal cord, showing the close pncking of cells and
the complexes of interdigitating membrane folds (arrows) between follicle cells.
X 5,500.
7 Fetal ovary at day 46. The picture shows a complex of deeply interdigitating membrane folds between follicle cells.
Th. Jeppesen
8 Primordial follicle, day 54.The follicle cells am Been to encircle the oocyte completely.
The complexes of interdigitating cell membranes have disappeared. One cell contains
abundant rough surfaced endoplasmic reticulum (arrow).X 5,000.
(FC)from primordial follicle (day 54). Arrows indicate bundles of
microfilaments. Germinal cell (GO.Zona pellucida (ZP).Basal lamina (BL).
9 Part of follicle cell
Th. Jeppesen
10 Part of follicle cell (day 66)from primordial follicle at high magnification showing a
bundle of 60-90 A thick microfilaments. Coated vesicle (CV).X 120,000.
11 Follicle cells, forming part of a primordial follicle (day 66). Bundle of microfilaments
is seen (arrow).A coated invagination of the cell membrane (CI)is seen in the region
of the zona pellucida (ZP).Oocyte (0).Basal lamina (BL). X 30,000.
Th. Jeppesen
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ultrastructure, guinea, pig, follicle, fetal, ovaries, cells
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