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Ultrastructure of the oocytes of the egyptian spiny mouse (Acomys cahirinus).

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Ultrastructure of the Oocytes of the Egyptian
Spiny Mouse (Acomys cahirinus) ’
YUAN-HSU KANG’ AND WINSTON A. ANDERSON
Laboratory of Cellular and Reproductive Biology, Department of Anatomy,
The Biomedical Center f o r Population Research, The University of
Chicago, Chicago, Illinois 60637
ABSTRACT
The oocytes of types 2 , 3 , 4 and 5 follicles from the normal spiny
mouse were examined with the electron microscope. Multiple juxtanuclear Golgi
bodies, mitochondria associated with flattened granular endoplasmic reticulum,
and large nucleus are the main features of the type 2 follicle oocyte. The numbers of mitochondria and Golgi apparati increase significantly at later stages.
Small mitochondria1 aggregates lacking “intermitochondrial cement” are seen
in the ooplasm of types 3, 4 and 5 follicles. “Lamellar complexes” comprising
two to six elongate flattened rough ER cisternae and intercisternal filaments begin to appear in the oocyte of the type 3 follicle. The intercisternal filaments may
be observed as punctate-, dashed-, and solid-lines in cross sections. In tangential
sections the filaments display a paracrystalline structure. In the type 4 follicle
oocytes, the “lamellar complex” becomes more extensive; polysomes and ribosomal fibrils are juxtaposed to the ‘‘lamellar complexes.” Bundles of ribosomal
fibrils are abundant in the ooplasm of the type 5 follicle. The origin of ribosomal filaments and the functional significance of “lamellar complexes” are
discussed.
The fine structure of the mammalian
granulosa cells and oocytes and ova have
been studied extensively in a variety of
animals: hamster (Weakley, ’66, ’67a,b;
Oder, ’65a,b; Hadek, ’66; Szollosi, ’67),
rabbit (Blanchette, ’61; Gondos, ’69; Hadek,
’63a, ’64; Motta, ’65; Pedersen and Seidel,
’72; Zamboni and Mastroianni, ’66a,b;
Trujillo-Cenoz and Sotelo, ’59; Merker,
’61), man (Baca and Zamboni, ’67; Baker
and Franchi, ’67; Hertig and Adams, ’67;
Hertig, ’68; Wartenberg and Stegner, ’60;
Stegner and Wartenberg, ’61), rat (Baccarini, ’71; Belt, ’62; Bjorkman, ’62;
Franchi, ’60; Franchi and Mandl, ’62;
Odor, ’60; Sotelo and Porter, ’59; VazquezNin and Sotelo, ’67), mouse (Byskov, ’69;
Chiquione, ’60; Hadek, ’63b; Wischnitzer,
’67; Yamada et al., ’57), guinea pig
(Anderson and Beams, ’60; Adams and
Hertig, ’64), dog (Szabo, ’67), bovine
(Priedkalns and Weber, ’68; Senger and
Saacke, ’70), sow (Bjersing, ’67), cat (Liss,
’64), elephant (Ogle et al., ’73), and rhesus
monkey (Hope, ’65; Crisp and Channing,
’72; Zamboni, ’74). Recently Zamboni
ANAT. REC., 182: 175-200.
(’72) and Szollosi (’72) have reviewed the
ultrastructure of the mammalian ova.
Despite the differences among species,
most mammalian oocyte possess some
common cytoplasmic features, such as
Golgi complexes, multivesicular bodies,
cortical granules, pinocytotic caveolae,
agranular and granular endoplasmic reticulum, free ribosomes, mitochondria, vesicular aggregates and coated vesicles. However, a few organelles, such as the annulate
lamellae, “yolk plates” and concentric
arrays of endoplasmic reticulum have been
observed in the oocytes of only a few
mammalian species. Annulate lamellae
have been described in man (Wartenberg
and Stegner, ’60; Adams and Hertig, ’65;
Zamboni et al., ’66; Baca and Zamboni,
’67; Hertig and Adams, ’67; Hertig. ’68;
Baker and Franchi, ’67), hamster (Weakley, ’69), and rabbit (Zamboni and Mastroianni, ’66a; Hadek, ’65). “Yolk plates”
Received Sept. 16, ’74. Accepted Dee. 9, ’74.
1 Supported, i n part, by grant M73.109 from the
Population Council and, in part, by USPHS grant HD
07110.
2 Supported bv a Dostdoctoral fellowship from NIH
training grant T01-HD00297.
175
176
YUAN-HSU KANG AND WINSTON A. ANDERSON
oocyte for a considerable distance as seen
in other species (Baca and Zamboni, '67;
Franchi, '60; Franchi and Mandl, '62;
Hertig and Adams, '67; Hope, '65; Chiquione, '60; Odor, '60; Yamada et al., '57).
The pregranulosa cells and the oocyte are
closely juxtaposed; however, a narrow
intercellular space, except at a few points
where macula adherens are formed (fig. 2
inset), surrounds the oocyte (fig. 3 ) .
Slightly dilated intercellular spaces which
accommodate the primordial (rudimentary)
granulosa cell processes and oocytic microvilli are also observed at intervals (fig. 2,
inset). On the surface of the oocyte there
are few pinocytotic caveolae, however
some fuzzy coated vesicles are seen in the
cytoplasm adjacent the oolemma (fig. 3).
A narrow rim of cytoplasm surrounds
the nucleus of the oocyte of type 2 follicles
(fig. 1 ). The agranular endoplasmic re ticulum is fairly developed and appears as
numerous pleomorphic vesicles. The granular endoplasmic reticulum is poorly deMATERIALS AND METHODS
veloped, and its cisternae are frequently
The ovaries of the young female Egyp- intimately associated with mitochondria.
tian spiny mouse were fixed for 1-2 hours
The oval or slightly elongate mitochonby immersion in 2.5% glutaraldehyde- dria, that are scattered throughout the
paraformaldehyde solution (Karnovsky, cytoplasm, possess dense matrix and few
'65) buffered with 0.1 M sodium cacodyl- cristae. Some mitochondria lie closely to
ate solution at pH 7.2. The tissues were both sides of the cisternal membranes of
then postfixed in 2% Os04 solution for 60 a tubular rough endoplasmic reticulum
minutes, dehydrated in graded alcohol solu- which often runs parallel to the oocyte surtions, and embedded in Epon (Luft, '61). face (figs. 1, 3 ) . In addition some mitoUltrathin sections for electron microscopy chondria may be partially enveloped by
were stained with aqueous uranyl acetate granular ER cisternae (fig. 1).
followed by lead citrate (Reynolds, '63) and
Elaborate paranuclear Golgi bodies comexamined with a Hitachi HU 11C electron posed of dilated cisternae and small vesimicroscope. For light microscopy, sections cles, are randomly distributed in the cyapproximately 1 thick were stained with toplasm between the oolemma and the
methylene blue.
nuclear membrane (figs. 1, 2).
Frequently undeveloped multivesicular
OBSERVATIONS
bodies which are surrounded by a constelOnly the follicles prior to the preantral lation of small vesicles and amorphous mastage, including type 2, 3, 4, and 5 follicles terial are seen in close vicinity of the Golgi
according to Pedersen's ('69, '72) classifi- apparatus (fig. 2). Typical multivesicular
cation, are considered in this paper.
bodies containing vesicles are present in
the cortical region of the oocyte (fig. 1 ) .
Type 2 follicle (primordial follicle)
Few membrane-bounded dense bodies reIn the primordial follicle of spiny mouse, sembling those described by Anderson ('72)
the young oocyte is surrounded by a single in rabbit oocyte and lipid droplets are usulayer of flattened pregranulosa cells which ally present in close relation to agranular
is in turn enclosed by a basal lamina (fig. endoplasmic reticulum and mitochondria
1 and inset). The extremities of the pre- (fig. 1 ) . Free ribosomes which appear in
granulosa cells may extend around the small clusters are dispersed throughout the
have been reported only to appear in the
cytoplasm of the mouse, rat, deer mouse
and hamster oocytes and ova (Enders and
Schlafke, '65; WeaMey, '68; Szollosi, '72).
A cytoplasmic inclusion similar to "yolk
plate" was also found in the young oocyte
of rhesus monkey (Hope '65) and in
human ova (Wartenberg and Stegner, '60).
Concentric arrays of endoplasmic reticulum are seen exclusively in the oocytes of
hamster, mouse, cat (Weakley, "68), and
rat (Kang, '74). Moreover, the configuration of the mitochondria in mammalian
oocytes also displays variation among species (Szollosi, '72).
In this paper the h e structure of the
Egyptian spiny mouse (Acomys cahirinus)
oocytes is compared with that of the other
mammalian species. In addition the development of the fibrillar arrays (ribosomal
fibrils) in the cytoplasm of the oocytes during the early stages of oogenesis is considered.
FINE STRUCTURE OF SPINY MOUSE OOCYTE
cytoplasm of the oocyte, while attached
ribosomes are sparsely and irregularly scattered along the cisternae which are often
affiliated with mitochondria.
The large spherical nucleus is centrally
located in the oocyte at this stage of development (fig. 1 ) . One or two pleomorphic
nucleoli which are composed of finely particulate material are seen centrally and
eccentrally in the nucleus. Multiple clumps
of fine, granular material interpreted as
heterochromatin are distributed around the
periphery of the nucleus (fig. 1). The nuclear pores are prominent and closed by a
diaphragm (figs. 1, 3).
Type 3 follicle (initial phase of
zona pellucida formation)
As the follicle grows, the oocyte becomes
enveloped by a single layer of cuboidal
granulosa cells (fig. 4 inset). The perivitelline space is not enlarged at this time.
However, cytoplasmic projections of granulosa cells and oocytic microvilli begin to
project into this space. A finely filamentous and/or amorphous material appears
in this narrow perivitelline space. At the
surface of the oocyte, pinocytotic vesicles
are numerous. In the cytoplasm, the numbers of mitochondria, Golgi apparati, multivesicular bodies, including undeveloped
and mature forms, have increased. The
cisternae of the nuclear envelope is dilated,
and the nuclear pores are apparent.
In slightly older follicles, the oocytes are
encompassed primarily by a single row of
cuboidal granulosa cells, however, two
layers of cells may be seen at one pole of
the oocyte. The perivitelline space now becomes dilated. Prominent cell processes,
oocytic microvilli and zona pellucida are
present in the perivitelline space (figs. 4,
5). However, the zona type of material is
incomplete and interrupted by thick processes of granulosa cells which are juxtaposed to the oocyte forming a wide macula
adherens (fig. 5 ) , similar to those observed
by Albertini and Anderson (’74).
In the cytoplasm of the oocyte, aggregates of mitochondria begin to appear.
Golgi complexes are frequently observed
between the mitochondria1 aggregates
(fig. 4).
177
The granular endoplasmic reticulum is
highly developed at this stage. In addition
to those associated with mitochondria,
stacks of curved and straight cisternae are
present in the ooplasm. These stacked
cisternae which are somewhat similar to
ribosomal bodies in the lizard oocytes
(Taddei, ’72, ’73), are the most prominent
cytoplasmic feature of the spiny mouse
oocyte. The number of cisternae in each
stack is variable, consisting most frequently of two or three cisternae (figs.
4, 6). Stacks consisting of as many as six
cisternae may be seen (fig. 9). The term
“lamellar complex” is designated to describe these stacks of granular endoplasmic reticulum. The width of the cisternae
in the “lamellar complex” show some variations, frequently dilated at the terminal
ends and occasionally in the middle section of the cisternae. The cisternal spaces
contain filamentous electron-opaque material, and infrequently disc-like bodies and
small vesicles may be encountered in the
widened portion of the cisternae (fig. 7).
Mitochondria and small clusters of vesicles
are also present in intimate association
with the outer aspects of the lamellar complex (figs. 7, 9).
In transverse sections of the “lamellar
complexes,” regardless of the number of
cisternae in each complex, all the cisternae
are separated by narrow intercisternal
spaces which contain electron-opaque cytoplasmic matrix averaging approximately
310 A in width, and a single strand of
ribosomes (or “intercisternal filaments”)
which are arranged parallel to the bordering cisternal membranes. The intercisternal filaments which are morphologically
analogous to the ribosome crystal sheets
(Byers, ’67; Barbieri et al., ’70; Maraldi
et al., ’70; Biagini et al., ’73) also display
three different views in transverse sections: ( a ) punctate-line view in which the
filament is formed by a chain of interconnected particles, which are about 150 h in
diameter and spaced 180 A apart from
one another, by thin strands of dense material (fig. 7, inset A) ; ( b ) dashed- or zigzagline form (fig. 7, inset B; fig. 9, inset b ) ;
and ( c ) spiral solid-line form (fig. 9, inset
a ) . The tangential sections of the intercisternal filaments show a paracrystalline
array (fig. 8).
178
YUAN-HSU KANG AND WINSTON A. ANDERSON
The Golgi apparatus, composed of few
stacked dilated saccules at the forming
face and some small vesicles at the maturing face, are located mainly in the cortical
region of the oocyte (fig. 4 ) .
Medium-sized membrane-bounded bodies
with electron-dense nucleoid, which are
analogous to nascent cortical granules,
now appear in the region near the Golgi
apparati and the “lamellar complexes.”
However, formation of cortical granules by
coalescence of small Golgi vesicles as described by Szollosi (’67) and Zamboni
(’70) was not observed at this stage.
The nucleus is large and spherical, and
slightly eccentric in the ooplasm. Heterochromatin material is not present at the
periphery of the nucleus. Chromatin particles are now evenly dispersed. One or two
nucleoli are present. Nuclear pores are
evident.
Type 4 follicle (completion of
zona pellucida formation)
As a complete envelope of zona pellucida
is formed, the oocyte is encompassed by
two layers of granulosa cells (fig. 10,
inset). The profiles of the granulosa cell
processes and microvilli derived from the
oocyte are numerous and clearly visible in
the zona pellucida. Macula adherens are
seen only at the contacts of granulosa cell
processes with the oocyte. Coated pinocytotic caveolae are evident on the surface
of the oocyte.
Small mitochondrial aggregates are seen
in the juxtanuclear and cortical regions of
the oocyte. However, electron-dense intermitochondrial substance or “intermitochondrial cement” (Andre, ’62) is not present
between mitochondria in the aggregates.
In some instances, the cristae have become concentric and formed a large central intercristal space containing electrondense matrix. Vesicles also begin to appear
within some of the mitochondria (fig. 11).
Most mitochondria still remain in close
association with the granular ER cisternae
(figs. 11, 12).
Multivesicular bodies, containing large
smooth-surfaced and small coated vesicles,
are surrounded by small spherical and
tubular vesicles and a thin layer of amorphous material (fig. 11, inset). In a few
cases, large bodies with incomplete limit-
ing membrane and granular and vesicular
electron-opaque contents are also seen in
the cortex of the oocyte (figs. 10, 12).
Cortical granules are sparsely present in
the oocyte (fig. 10). Golgi apparati are
numerous and mostly situated in the cortical region, and are constituted by curved
saccules and vesicles in the concave region
(fig. 11).
Small aggregates of free ribosomes are
scattered over the ooplasm as seen in the
previous stage. Spiral and linear complexes of ribosomes are seen along the
outermost cisternal membranes of the
“lamellar complex” (figs. 14, 15).
The “lamellar complex” of the granular
endoplasmic reticulum is now extensively
developed. Single granular ER cisternae
and the complexes, primarily composed of
two to three strands of granular ER cisternae, occupy the ooplasm (figs. 13, 14).
The intercisternal filament, in some instances, shows continuity with the neighbor filament along the membrane of the
dilated end of the cisterna (fig. 13, inset).
Type 5 follicle (pre-antral follicle)
The oocyte is enclosed by a thicker zona
pellucida layer which is in turn encircled
partially by at least three layers of granulosa cells (fig. 16, inset). Numerous transverse sections of microvilli are seen in the
zona pellucida around the oocyte. Cytoplasmic processes of granulosa cell form
intercellular junctions with oocyte at deep
indentations on the oocyte surface.
Cortical granules become more numerous at this stage of development. Large
vacuoles with thin filamentous contents
may be seen occasionally in the cortical
region. Mitochondria1 aggregates lacking
“inter-mitochondria1 cement” are seen in
the cortical and subcortical regions of the
oocyte (fig. 16). Frequently the mitochondria are accompanied by some dense bodies
without limiting membranes, and are associated with rough ER cisternae (fig. 17).
The sizes of the mitochondria are variable.
The mitochondrial cristae are scant and
mostly concentric. Vesicles also appear in
the matrix of some of the mitochondria.
The granular endoplasmic reticulum
which is often associated with mitochondria appears to show the relationship be-
FINE STRUCTURE OF SPINY MOUSE OOCYTE
tween ribosomes and the formation of ribosomal fibrils (fibrillar arrays). In cross
and oblique sections of these single-strand
ER cisternae, some ribosomes are irregularly studded along both sides of the cisternal membranes (fig. 17), moreover,
prominent ribosomes arranged in singlerow fashion are present along the cisternal
membranes (figs. 17, 18). Ribosomal fibrils also appear along the cisternae shown
in figures 17 and 18). Hexagonal paracrystalline structure is seen in the tangential section of a cisternal membrane (fig.
18). Few polysome helices may be seen
close to the cisternal membrane (fig. 19).
Golgi apparati composed of slender saccules and vesicles containing amorphous
material are scattered near the oolemma
and among the mitochondria in the cortical
region of the oocyte (fig. 20).
In addition to those mitochondria-associated granular ER cisternae, the “lamellar
complexes” are more extensive and profuse than the previous stage. They exhibit
high variations i n configuration, and are
often interspersed by smooth-surfaced dilated vesicles and amorphous granules.
Predominantly they are straight, less frequently are curved at one end or compressed circle (fig. 21). In the older oocytes
more frequently the cisternae break into
fragments, and are associated with long
straight ribosomal fibrils (fig. 21). In the
transverse and oblique sections, the ribosomal fibrils consist of linear and sheetlike arrays of interconnected particles
which are about 110 A in diameter, spaced
190 to 290 A apart from center to center,
or exhibit periodicity at intervals of approximately 170 A. The fibrils in stack
usually run parallel to each other, and are
spaced 360 to 650 A and interconnected
by transverse strands (fig. 21). Stacks of
ribosomal fibrils numbering from two to
seven which are independent from the
“lamellar complexes” are now dispersed
widely throughout the ooplasm (fig. 16).
Two types of multivesicular bodies occur
in the ooplasm at this stage. The first type
which is often situated adjacent to Golgi
apparatus contains numerous small vesicles, but no vesicles and dense material
encircle it (fig. 16). Another type is larger
than the first type and contains amorphous
179
material and numerous smooth-surfaced
and coated vesicles, and is surrounded by
some small vesicles and dense material.
Large fuzzy coated invaginations and
finger-like projections are also seen on the
surface of the large type multivesicular
body.
DISCUSSION
Golgi apparatus
The development of the Golgi apparatus
in the spiny mouse oocyte shows strong
resemblance to mouse, rat, guinea pig,
rabbit, rhesus monkey, and man (Adams
and Hertig, ’64; Anderson and Beams, ’60;
Blanchette, ’61; Franchi and Mandl, ’62;
Hope, ’65; Odor, ’60; Sotelo, ’59; Sotelo and
Porter, ’59; Weakley, ’66; Yamada et al.,
’57; Zamboni, ’72). In the oocyte of the
spiny mouse primordial follicle (type 2),
the large Golgi apparatus lies in a close
juxtanuclear position and consists of few
dilated saccules and numerous small vesicles. Later in the unilaminar follicle (type
3 ) the Golgi complex proliferates and lies
between mitochondria1 masses in the cortical and subcortical regions of the oocyte.
In the oocytes of the subsequent stages
(types 4 and 5 ) , the Golgi apparati consisting of curved stacks of saccules and
vesicles containing amorphous material
are mainly situated in the cortical region
and also in close association with mitochondria.
Several roles have been proposed for the
Golgi complex in the developing oocytes.
It is involved in the formation of the zona
pellucida (Odor, ’60; Adams and Hertig,
’64; Hope, ’65; Kang, ’74) and cortical
granules (Adams and Hertig, ’64; Baca
and Zamboni, ’67; Szollosi, ’67; Zamboni,
’70), and in the synthesis of mucopolysaccharides (Kang, ’74). According to our
observations on the spiny mouse oocytes,
it is plausible to suggest that the Golgi
complex is involved in the formation of
the zona pellucida and cortical granules.
A “yolk nucleus” (Balbiani body) which
includes a large mass of Golgi vesicles and
clumps of dense amorphous material (Anderson and Beams, ’60; Zamboni and Mastroianni, ’66a; Hertig and Adams, ’67) is
not seen in the corresponding stage of the
spiny mouse oocyte.
180
YUAN-HSU KANG AND WINSTON A. ANDERSON
Cortical granules
Cortical granules which were first observed by Austin (’56) in the hamster egg
are frequently present in the cortical cytoplasm of mammalian oocytes (Hadek, ’63a;
Adams and Hertig, ’64; Hope, ’65; Szollosi,
’62; Weakley, ’66; Baca and Zamboni, ’67;
Zamboni, ’70). In the spiny mouse oocyte,
round membrane-bounded granules, containing electron-dense material, first appear
in the cortical region of type 3 follicles
that have prominent Golgi apparati. Later
as soon as a complete layer of zona pellucida is formed, mature cortical granules
are sparsely distributed in the cortex of the
oocyte. In type 5 follicle oocytes more cortical granules are produced and may appear in small groups.
The formation of cortical granules as
proposed by Adams and Hertig (’64) in
hamster egg, Szollosi (’67) in mouse and
hamster eggs, Zamboni (‘70, ’72) in human
and mouse oocytes was not observed in the
spiny mouse oocytes. However, fusion of
small vesicles containing electron-dense
material, which is possibly responsible for
the formation of cortical granule, is evident
at the vicinity of Golgi complexes and the
“lamellar complexes.”
Cortical granules of mammalian oocytes
are presumably involved in the “cortical”
or “zona” reaction during sperm penetration (Hadek, ’63a; Szollosi, ’67). Cortical
granules have been shown acid phosphatase positive in sea urchin eggs (Dalcq,
’65) and in polyclad tubellarian (Prosthecmaneus floridanus) eggs (Boyer, ’72).
In contrast, W. Anderson (’68) and
E. Anderson (’72) reported that the cortical
granules of the sea urchin and mammalian
egg were respectively acid phosphatase
negative. Recently Vacquier et al. (’72)
and Schuel et al. (’73) reported that a
trypsin-like protease found in the cortical
granules of sea urchin eggs may be involved in the elevation of fertilization
membrane. Moreover Gwatkin et al. (’73)
found a similar enzyme which causes the
zona reaction in the cortical granules of
hamster and mouse eggs.
Mitochondria and endoplasmic
reticulum
The association of mitochondria with
cisternae of granular ER is prominent in
the oocytes of spiny mouse. Mitochondria-ER associations begin to appear in
type 2 follicle oocytes in which several
mitochondria are closely juxtaposed to the
cisternae of elongate tubular rough ER. In
later stages, small cisternae with sparsely
studded ribosomes or with the associated
ribosomal fibrils are present between mitochondria. In other species such associations are also present, however ribosomal
fibrils are completely absent along the cisternal membranes (Szollosi, ’69, ’72; Zamboni, ’72; Lanzaveccia and Mangioni, ’64).
The functional significance of mitochondria ER complexes is unclear. Fawcett
(’66) suggested that ER-mitochondria associations may be an example of transient
juxtaposition of the mitochondria to a local
site of energy utilization. In the case of
spiny mouse, one feasible interpretation of
the ER-mitochondria-ribosomal fibril association may be that the mitochondria partially provide the granular endoplasmic
reticulum with energy required for the formation and crystallization of polysomes
which subsequently develop into crystallized ribosomal fibrils along the sides of
the cisternae.
The endoplasmic reticulum in the mouse
(Yamada et al., ’57), rat (Sotelo and
Porter, ’59; Odor, ’60j , rabbit (Blanchette, ’61), hamster (Weakley, ’68), man
(Wartenberg and Stegner, ’60) is present
only in meager amounts, however, it is extensive in guinea pig (Adams and Hertig,
’64). In the spiny mouse, the endoplasmic
reticulum is moderately developed in the
early stage, later the granular endoplasmic
reticulum becomes extensive and organized
in a “complex” form. In the above mentioned species, no oocytes have been found
to have ‘lamellar complex” of granular
endoplasmic reticulum as seen in the spiny
mouse. Recently a similar structure has
been reported in the oyster oocyte (Daniels
et al., ’73).
Concentric arrays of endoplasmic reticulum have been reported in the oocytes of
rat (Kang, ’74), hamster, mouse and cat
(Weakley, ’68). There are not such arrays
found in the spiny mouse oocyte. Szabo
(’67) suggested that concentric arrays of
endoplasmic reticulum is involved in yolk
formation in dog oocyte.
FINE STRUCTURE OF SPINY MOUSE OOCYTE
Ribosomal fibrils
Porte and Zahnd (’61) first described in
the lizard Lacerta stirpium oocyte a lamellar structure which was later referred to
by Ghiara and Taddei (’66), and Taddei
(’72) as the ribosomal body. This structure
was thought to function in the regulatory
mechanism of protein synthesis (Taddei
et al., ’73). Moreover, Zahnd and Porte
(’63) reported the presence of a tubular
paracrystalline structure in the oocyte of a
turtle (Tesudo ermania). The lamellar
paracrystalline arrays of ribonucleoprotein
were also found in the ooplasm and nucleus of the developing oocytes of the ostracod (Cypridopsis vidua) (Reger, ’64; Reger
et al., ’65).
The occurrence of such paracrystalline
arrays in the mammalian oocytes was first
described as “fibrous elements” by Enders
and Schlafke (’65) in the oocytes and
blastocysts of mouse, rat, deer mouse and
hamster. Enders and Schlafke (’65) also
found that the “fibrous elements” are soluble in permanganate fixative but well preserved by glutaraldehyde fixation. These
fibrous elements are thought to be proteinaceous in nature. Similar structures called
“paracrystalline lamellae” were thought to
participate in the development of yolky
substance in ovarian and tuba1 ova of rats
and hamsters (Szollosi, ’65). Hadek (’66)
named the same structure in the hamster
oocyte “cytoplasmic whorls.” Weakley (’66,
’67a, ’68) described the paracrystalline arrays as “cytoplasmic non-membranous lamellae” in rat, hamster and mouse oocytes;
these structures are absent in cat and guinea pig oocytes (Weakley, ’68). She also
made a significant study on the nature of
the cytoplasmic lamellae and found that
they were digested by pepsin (’67). More
recently “yolk plates” on the basis of their
proteinaceous nature, were thought to represent the paracrystalline lamellae in the
mammalian ooplasm by Szollosi (’72).
Protein crystalloids which are probably morphogenetically analogous to “yolk
plates” have been reported in the young
oocytes of rhesus monkey (Hope, ’65) and
man (Wartenberg and Stegner, ’60).
In the ooplasm of hamster, mouse and
rat the “yolk plates” commence to appear
by the time the oocytes are enclosed by a
single layer of cuboidal granulosa cells,
181
they proliferate and become extensive at
later stages (Weakley, ’68). In the rat
primordial follicle oocytes, however, periodic beaded filaments resembling “yolk
plates” have been observed (Kang, ’74). In
the spiny mouse oocyte the periodic beaded
filaments which are probably the precursors of ribosomal fibrils first appear in the
intercisternal spaces by the time the oocyte
is encompassed by a single layer of cuboidal granulosa cells (type 3 follicles) ; later
they become more extensive and start
separating from the ER lamellar complexes
(in type 4 follicle). Finally numerous
stacks comprising two to seven fibrils per
stack become widely distributed at the time
the oocytes have become enveloped by three
granulosa cell layers (type 5 follicle).
The arrangement and periodicity of the
“yolk plates” differ slightly among species.
In the three-layer hamster follicles, the
fibrils frequently appear as two parallel
lines transversely connected by dense
strands at intervals approximately 400 A
(Weakley, ’68). In the rat, the “yolk plates”
are more clearly delineated in the younger
oocytes (type 3 follicles) ; the periodicity is
evident and measuring approximately 350
A (Szollosi, ’72). Subsequently the structures are obscured by the presence of electron-dense amorphous material and packed
in large stacks containing numerous fibrils
in cross sections (Weakley, ’68; Szollosi,
’72). In the mouse oocytes stack form
“yolk plate” is made of cross-linked fibrils,
with a 350 A main periodicity (Weakley,
’68; Burkholder et al., ’71; Szollosi, ’72).
In the spiny mouse oocytes, cross sections
of the “yolk plates” commonly appear to
be long and rectilinear, particularly those
associated with the cisternae of granular
endoplasmic reticulum. Single and stacks
of fibrils have been observed. The single
fibrils abut the cisternal membranes of
the “lamellar complex,” whereas the stacks
are in general scattered over the ooplasm.
The periodicity of the fibrils, measuring
190 to 290A is very prominent in transverse sections. In the bundle form each
fibril is interconnected by thin cross bridges
that are spaced 360 to 650 A.
The origin of “yolk plates” in the rat
and hamster has not been observed probably due to its rapid development, and
also no other organelle appears to be in-
182
YUAN-HSU KANG AND WINSTON A. ANDERSON
volved in its formation, Nevertheless
Weakley (’68) suggested that the cytoplasmic lamellae in the hamster ooplasm are
possibly developed from strands of fine
filaments. Zamboni (’70) has reported that
the fibrillar arrays in the mouse oocytes
appear to form from polysomes: “At first
the ribosomes become arranged in a curvilinear pattern and then they fuse giving
rise to a typical fibril which may subsequently increase in length by addition of
other ribosoma1 templates .”
The ribosomal fibrils of the spiny mouse
oocyte show a great similarity to the ribosome crystals of hypothermic chick embryos (Byers, ’67; Maraldi and Barbieri,
’69; Barbieri et al., ’70; Biagini et al., ’73)
and to the crystalline polysomes in ostracod oocytes (Reger, ’64; Reger et al., ’65).
In the spiny mouse oocytes, two types of
polysomes, linear and curvilinear forms,
have been observed on the cisternal membranes of the “lamellar complexes” which
are often accompanied by long straight
ribosomal fibrils on the sides. Another type
of polysome which is tortuous and attached
to the cisternal membranes or free in the
cytoplasm, is also present by the time ribosomal fibrils begin to appear. Furthermore,
irregular-shaped smooth-surfaced vesicles
which are possibly derived from the disintegration of the cisternae of the “lamellar complex” are particularly abundant between the cisternae during the formation
of ribosomal fibril. Therefore, our observations seem to indicate that the “lamellar
complexes” of granular endoplasmic reticulum are very likely directly involved in the
formation of ribosomal fibrils. It is tentatively suggested that free ribosomes, that
gather along the cisternal membranes of
the “lamellar complex,” become arranged
in a linear pattern and then crystallize into
“yolk plates” or ribosomal fibrils. Subsequently the cisternae move apart from one
another and break into small dilated vesicles. The cisternae of the “lamellar complex,” therefore, may play an important
role in the accumulation, organization and
crystallization of the ribosomes. The origin
and the mechanism of crystallization of
the ribosomes are unknown. Biagini et al.
(’73) suggested that the crystallized ribosomes in the hypothermic chick embryos
are not derived from polysomes but cyclically exported from nuclei during mitosis.
The functional significance of “yolk
plates” in the mammalian oocytes remain
obscure. Yet, Enders and Schlafke (’65)
found that following the sperm penetration
the “yolk plates” are gradually reduced in
number while in delayed blastocyst they
disappeared completely. Zamboni et al.
(’66) proposed that crystalline inclusions
in human ovum represent ooplasmic yolk,
in addition, “yolk plates” have been proved
to be largely protein in nature (Enders
and Schlafke, ’65; Szollosi, ’67; Weakley,
’67); thus they may serve as an important
nutritive source for the early development
of zygote. Furthermore, Weakley (’67) reported that the cytoplasmic lamellae might
function as a “temporary endoplasmic
reticulum” for protein transport or serve
as sites for the location of enzyme systems
and for protein synthesis. Recently Burkholder et al. (’71) suggested that in mouse
oocytes ribosomal fibrils are storage forms
of ribosomes which are released for protein synthesis during early cleavage. The
role of the scattered free tortuous polysome
helices cannot be determined at the present
time.
Multivesicular bodies (MVB)
Odor (’60, ’65a) has noticed two types
of multivesicular bodies, including single
unit and group forms, in rat and hamster
oocytes. This is in accordance with observations in other mammalian species. Generally single units are more frequently observed in the immature oocytes (primordial
follicles), whereas group forms are common in the primary and secondary oocytes
and in the fertilized or dividing ova
(Yamada et al., ’57; Sotelo and Porter, ’59;
Franchi and Mandl, ’62; Anderson and
Beams, ’60; Wartenberg and Stegner, ’60).
In contrast, in the spiny mouse group
forms are frequently seen in the younger
oocytes (type 2 follicles) and the single
units containing numerous MVB (multivesicular body) vesicles are predominant in
the maturing oocytes (types 4 and 5 follicles).
Four hypotheses have been proposed to
explain the origin of the multivesicular
body. It has been suggested that a multivesicular body is formed by the penetration
FINE STRUCTURE OF SPINY MOUSE OOCYTE
of small vesicles through the limiting membrane of a phagolysosome (Novikoff et al.,
’64; Novikoff and Shin, ’64; Gordon et al.,
’65). The second theory suggests that the
MVB forms by autophagy of clusters of
vesicles (Friend, ’69; Martin and Spicer,
’ 7 3 ) . The third theory is a combination of
the first two theories (Friend and Farquhar,
’67; Friend, ’69), suggests that the MVB
vesicles are added to the multivesicular
body by a process of budding from the
limiting membrane of the body instead of
penetration. Our observations on the spiny
mouse oocytes appear to show strong support to the third theory. The last theory
suggests that some multivesicular bodies
may arise from “cup-like” bodies which
participate in heterophagy (Holtzmann and
Dominitz, ’68).
The role of multivesicular body in the
mammalian oocytes is ambiguous. It has
been suggested that multivesicular bodies
may be involved in the formation of “centrosphere masses” of meiosis (Sotelo and
Porter, ’69) and yolk platelets (Stegner
and Wartenberg, ’61). The presence of acid
phosphatase and the incorporated horseradish peroxidase in the multivesicular
bodies in guinea pig and mouse oocytes
suggests that they may be considered
phagolysosomes (Anderson, ’72). Furthermore Martin and Spicer (’73) recently
stated that the multivesicular body in the
syncytiotrophoblast of human term placenta may function in selective hydrolysis
and transport of endocytosed protein.
ACKNOWLEDGMENT
The authors wish to express their gratitude to Dr. L. Zamboni (Harbor General
Hospital, Torrence, California) for his
valuable comments on the manuscript.
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Abbreviations
BM, basal lamina
CG, cortical granule
CV, coated vesicle
M, mitochondria
MVB, multivesicular body
N, nucleus
DB, dense body
FGC, granulosa cell
GC, Golgi apparatus
LC, “lamellar complex”
LD, lipid droplet
Ncl, nucleolus
NP, nuclear pore
PFC, cytoplasmic process
of granulosa cell
PS, perivitelline space
rER, granular endoplasmic
reticulum
RF, ribosomal fibril
sER, agranular endoplasmic
reticulum
TER, tubular smooth endoplasmic reticulum
VA, vesicular aggregate
ZP, zona pellucida
PLATE 1
EXPLANATION O F FIGURE
1
A type 2 follicle is shown here. A single layer of flattened granulosa
cells (FGC) immediately surround the oocyte. Golgi bodies (GC),
mitochondria, granular endoplasmic reticulum (rER), lipid droplets
(LD), dense bodies (DB), vesicular aggregate (VA), and multivesicular body (MVB) are present in the cytoplasm of the oocyte. Nucleoli
(Ncl) are seen in the nucleus and nuclear pores (arrows) are prominent. Inset is a light micrograph of the type 2 follicle. X 8,300.
FINE STRUCTURE OF SPINY MOUSE OOCYTE
Yuan-Hsu Kang and Winston A. Anderson
PLATE 1
187
PLATE 2
EXPLANATION OF FIGURES
188
2
Type 2 follicle oocyte. A multivesicular body ( M V B ) is closely associated to the Golgi apparatus (GC). Inset shows intercellular junction and space between oocyte and granulosa cell (FGC). x 15,500;
inset x 26,250.
3
High magnification of a region of a type 2 follicle oocyte showing
the association of mitochondria ( M ) with granular endoplasmic
reticulum (rER). x 29,300.
4
Type 3 follicle oocyte. Zona type of material ( Z P ) begins to appear
in the perivitelline space. Mitochondrial aggregates, Golgi bodies
(GC), and “lamellar complexes” ( L C ) are seen in the ooplasm.
Arrows show the juxtaposition of adjacent mitochondria. A light
micrograph of a type 3 follicle is shown i n the inset. x 9,000.
FINE STRUCTURE OF SPINY MOUSE OOCYTE
Yuan-Hsu Kang and Winston A. Anderson
PLATE 2
189
PLATE 3
EXPLANATION O F FIGURES
190
5
Type 3 follicle. A large cytoplasmic process (PFC) derived from a
granulosa cell (FGC), and zona pellucida ( Z P ) are seen in the perivitelline space. Coated vesicle (CV) and Golgi complex (GC) are
present in the cortical ooplasm X 29,300.
6
“Lamellar complexes” (LC) comprising several rough ER cisternae,
Golgi bodies (GC), and mitochondria are present in the cortical
regions of the oocyte of a type 3 follicle. X 10,400.
7
High magnification of a “lamellar complex” showing the punctate
(inset A ) and dashed-line (inset B) views of the intercisternal filaments. Arrows indicate the subunits of the filaments. x 30,520;
insets A,B, x 100,440.
8
A tangential section of a “lamellar complex” showing the paracrystalline arrays of the intercisternal filaments. X 52,000.
FINE STRUCTURE OF SPINY MOUSE OOCYTE
Yuan-Hsu Kang and Winston A. Anderson
PLATE 3
191
PLATE 4
EXPLANATION O F FIGURES
9
A more elaborate “lamellar complex” consisting of six rough ER
cisternae is seen i n the cortical region of the oocyte of a type 3 follicle. The paracrystalline structure with fine hexagonal lattice of the
intercisternal filaments is evident. The solid ( a ) and punctate (b)
views of intercisternal filaments are shown in the inset. x 24,000;
inset X 38,550.
10 The type 4 follicle oocyte is enveloped by a complete layer of zona
pellucida (ZP). Cortical granules (CG) are now present in the cortical
and subcortical regions. Numerous “lamellar complexes” (LC) are
present in the ooplasm. Inset shows light micrograph of the corresponding stage. x 25,000.
FINE STRUCTURE OF SPINY MOUSE OOCYTE
Yuan-Hsu Kang and Winston A. Anderson
PLATE 4
193
PLATE 5
EXPLANATION O F FIGURES
11 Mitochondria1 aggregates, polysomes (thin arrows), Golgi bodies
(GC), tubular smooth endoplasmic reticulum (TER), and “lamellar
complexes” (LC) are shown in a type 4 follicle oocyte. Inset shows a
multivesicular body (MVB) with coated invaginations (arrows) on
the surface, and the affiliated aggregate of vesicles ( V A ) . x 142,500;
inset x 20,000.
12
Cortical region of a type 4 follicle oocyte contains mitochondrial
aggregates, numerous polysomes, and a large body containing dense
granules (thick arrow). x 11,500.
13 Transverse section of “lamellar complexes” showing the intercisternal filaments and the associated ribosomal fibrils. A cluster of
tubular smooth endoplasinic reticulum (TER) is seen adjoining the
complex. In the inset, the arrows indicate the intercisternal filaments
are connected to one another around the dilated end of a cisterna.
X 18,000; inset X 19,000.
194
FINE STRUCTURE OF SPINY MOUSE OOCYTE
Yuan-Hsu Kang and Winston A. Anderson
PLATE 5
195
PLATE 6
EXPLANATION O F FIGURES
196
14,15
Type 4 follicle. Transverse sections of “lamellar complexes” showing the separation and disintegration of the cisternae. Note the
ribosome-like fibrils and remnants of cisternae. x 16,800, x 14,250.
16
Numerous cortical granules (CG), multivesicular body (MVB ),
Golgi apparatus (GC), mitochondria, and bundles of ribosomal
( R F ) are seen in the cortical and subcortical regions of a n oocyte
of a type 5 follicle. Inset is the light micrograph of the corresponding stage. X 17,000.
FINE STRUCTURE OF SPINY MOUSE OOCYTE
Yuan-Hsu Kang and Winston A. Anderson
PLATE 6
197
PLATE 7
EXPLANATION O F FIGURES
198
17-19
Small portions of type 5 follicle oocyte showing the intimate
association of mitochondria with granular ER cisternae. Regularly
arranged ribosomes (thick arrows) are present on the cisternal
membranes (figs. 17, 18, 19). In figure 18, hexagonal paracrystdline structure (thin arrow) is seen in the tangential section of a
cisternal membrane. A curvilinear polysome (thin arrow) is seen
close to a cisternal membrane (fig. 19). X 37,520.
20
Cortical portion of type 5 follicle oocyte showing the well-developed
Golgi bodies and mitochondria. x 14,000.
FINE STRUCTURE OF SPINY MOUSE OOCYTE
Yuan-Hsu Kang and Winston A. Anderson
PLATE 7
199
FINE STRUCTURE OF SPINY MOUSE OOCYTE
Yuan-Hsu Kang and Winston A. Anderson
EXPLANATION OF FIGURE
21
200
Numerous ribosomal fibrils, remnants of cisternae, and “lamellar
complexes” (LC) are seen in the ooplasm of an older type 5 follicle
oocyte. x 16,200.
PLATE 8
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ultrastructure, spina, oocytes, mouse, egyptian, acomys, cahirinus
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