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A Comparative Electron Microscopic Study on Ehrlich Ascites
Tumor Cells, Yoshida Sarcoma Cells, and Human
Cancerous Peritonitis Ascites Cells
G. YASUZUMI
ANDR. SUGIHARA
(Laboratory for Electron Microscope Research, Department
It is known that the Ehrlich ascites tumor
is of epithelial origin, while the Yoshida sarcoma
originates from the reticuloendothelium
(13). The
present paper deals with a comparative electron
microscopic study of uninfected Ehrlich mouse
ascites tumor (EAT) cells, Yoshida sarcoma (YS)
cells, and human cancerous peritonitis
ascites
(HCPA) cells. A morphological
analysis of the
EAT by electron microscopy had already revealed
virus-like particles in the ground substance of
the cytoplasm (5, 6, 8, 9, 12). Recent progress
achieved via the electron microscope in the study
of the submicroscopic structure of the uninfected
EAT cells renewed interest in the virus-like par
ticles associated with the endoplasmic reticulum
(1, 3, 11). Although Wessel and Bernhard
(8)
have recently demonstrated
a fibrous structure
in the YS cells, they have stated that definite
discrimination
between EAT and YS by means
of electron microscopy is impossible.
During the course of a series of electron micro
scope studies on the ascites cells mentioned above,
carried out in this laboratory, an obvious differ
ence was observed between them: virus-like par
ticles appeared primarily in the endoplasmic retic
ulum but occasionally in nuclei of EAT cells;
fibrous elements, as well as spindle-like bodies
of varying size, appeared in the ground substance
of the cytoplasm of YS cells; division into endoand ectoplasm occurred in HCPA cells.
MATERIALS
AND METHODS
The ascites fluids of 7-10 days' inoculation age
of EAT, 4-5 days' inoculation age of YS, and of
HCPA were used in the present study. The patient
was a 36-year-old housewife who had received
treatment following a diagnosis of cancerous peri
tonitis at Nara Medical College Hospital. Para
centesis was performed, with removal of 5000
cc. of bloody fluid, with specific gravity of 1.010;
there was a positive Rivalta reaction; culture
Received for publication April 24, 1958.
of Anatomy,
Nara Medical College,'Nara
Pref., Japan)
gave no growth. An operation was performed
at the hospital, revealing a tumor the size of
a hen-egg in the pyloric region. The pancreas
and retroperitoneal
regions showed diffuse metastatic inflammation which made gastrectomy im
possible.
Approximately
0.5 ml. of ascites fluid was re
moved by capillary pipette from the peritoneal
cavity and placed immediately
in 1 per cent
osmium tetroxide buffered at pH 7.3 with veronalacetate. After fixation for 30 minutes the cells
were directly dehydrated,
without being washed
in distilled water, in a series of increasing concen
trations of ethyl alcohol and embedded in a mix
ture of methyl methacrylate
and n-butyl methacrylate. Polymerization
was carried out at 48°C.
Sections were cut
glass knives. They
film-coated copper
without removal
an Akashi electron
on a Shimadzu microtome with
were then mounted on collodion
specimen grids and examined,
of the embedding plastic, in
microscope model TRS-50.
RESULTS
Uninfected Ehrlich mouse ascites tumor cells.—
The cytoplasmic structure is individually variable,
but it appears that the mitochondria
enlarged
to vacuolization,
that the rough-surfaced
endo
plasmic reticulum
(4) decreased, and that the
cytoplasmic dense particles characteristic
to the
EAT increase, as inoculation age proceeds.
The rough-surfaced
endoplasmic reticulum is
not particularly well developed, but an even great
er number of minute granules are evenly distrib
uted through the cytoplasm, giving it a finely
stippled appearance (Figs. 1-3). Mitochondria oc
cur in all regions of the cell but are particularly
numerous at the periphery of the cell center.
They tend to be larger than usual and finally
undergo vacuolization,
forming a ring structure
(Figs. 1-3). The Golgi complex has the same
basic structure as that of other epithelial cells,
being made up of aggregations of small vesicles
1167
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1168
Cancer Research
and parallel arrays of smooth membranes
or
ganized into two or more groups that are found
closely attached to a lipide droplet (Fig. 1.)
The nucleus is enveloped
in the doublestructured nuclear membrane. The nucleus is often
characterized by a deep indentation of its surface
(Fig. 4) or intranuclear
canals continuous with
the inner of the nuclear membranes
(Fig. 2).
The karyoplasm consists of a matrix of low density
containing fine granules of three or more kinds
that differ in size and density and in their state
of aggregation (Figs. 2 and 4).
The most common of the abnormal structures
is a particle of uniform size and distinctive form
found in considerable numbers in the cytoplasm
and occasionally in the nucleus. The intracytoplasmic virus-like particles are detectable in the
lumina of the endoplasmic reticulum, being fre
quently encountered in small or large groups (Figs.
1 and 3). It has been found that the particles pos
sess a characteristic
internal structure consisting
of a core of low density, 15-25 niju in diameter,
surrounded by a dense shell 20-30 ra.fi thick, show
ing an over-all diameter ranging from 55 to 75
mß (Fig. 2). It is interesting that the obliquely
sectioned tubular endoplasmic reticulum reveals
continuity between the agranular portion of the
membrane surrounding the particles and the ad
jacent granular portion which can be definitely
identified as rough-surfaced endoplasmic reticulum
(Fig. 2). The virus-like particles are found in the
nucleus, being spheroidal in shape and 80-140
im* in diameter. They consist of a dense capsule
about 12 imj thick enclosing a clear central zone
40-70 imt in diameter, which is of very low density
and gives the appearance
of a central cavity.
Within this cavity is a round or oval, dense
body 56 imt or less in diameter.
In some
planes of section the inner body is completely
surrounded
by a clear zone and thus appears
to be central, but when cut in other planes
it is clear that the inner body is eccentrically
placed and is fixed on one side to the inner aspect
of the capsule. The intranuclear particles do not
occur individually
as they do in the cytoplasm
but are geneally closely associated in a cluster.
Such aggregations of particles are situated near
or within the vesicle appearing in the nucleus
(Fig. 4).
Yoshida albino rat sarcoma cells.—The cell cen
ter consists of an aggregation of single membranelimited vesicles with varying size and varying
electron density. The cytoplasmic matrix is of
rather low density.
The rough-surfaced
endo
plasmic reticulum is not well developed. One or
more spherical or irregularly shaped particles are
Vol. 18, November,
1958
occasionally found within the vesicles. To date
it has been possible to assemble from the electron
micrographs a sequence of formation stages which
would possibly be a clue to the origin of these
particles. Most of them are less dense and smaller
than those found in the EAT cell. A few circular
or prolonged mitochondria with a typical internal
structure are found surrounding
the cell center
(Figs. 5 and 6).
A second type of abnormal structure
found
in the cytoplasm is one or more bundles of con
spicuous fibrous elements ca. 150 A in thickness
(Figs. 5-7). Such elements are never seen in normal
albino rat ascites cells or in EAT cells. They are
quite common, however, in the cytoplasm of YS
cells. In Figure 7 the internal structure of the
majority of mitochondria
surrounding the fibrous
elements is in a state of dissolution. A further
sign of pathological alterations is the appearance
of the lipide body.
A third type of abnormal structure found in
the cytoplasm is short or long spindle-like bodies.
Figure 8 is an electron micrograph of the short,
spindle-like profile, 1.3 fi in length and 0.26 p
in width, which is composed of fine vesicular
masses with moderate density, being surrounded
by a few pairs of membranes
in more or less
parallel arrangement.
The cross-sectioned
profile
in an oval shape, the moderate-sized
one being
1.0-1.6 p in diameter (Fig. 9), shows a few vesicles
of varying size and varying density embedded
in an apparently
homogeneous substance of low
opacity. The elongate body, more than 4.0 ß
in length and 0.6 /¿in greatest width (Fig. 10)
is composed of vesicles of varying size which
contain a homogeneous
mass of low density or
a few granules about 20 ra.fi in diameter. It is
characteristic
that the peripheral portion of the
profile is surrounded
by membranes
in a more
or less parallel arrangement,
usually with a some
what wavy course. Mitochondria
are swollen and
occasionally found along the body.
Human cancerous peritonitis ascites cell.—Small
sized or vacuolized mitochondria
and a few elec
tron-lucent vesicles of varying size are found sur
rounding the nucleus, which is situated in the
central part of the cell. The endoplasmic reticulum
is occasionally visible in a linear array. The nu
clear chromatin free of dense particles is composed
of fine granules aggregated into irregularly shaped
masses of varying size and indefinite outline; these
occur in all parts of the nucleus. Nucleolonemata
are not clear in the irregularly shaped nucleolus
(Fig. 11).
In the cell, in which the nucleus is shifted
toward the peripheral part of the cell and trans-
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YASUZUMIAND SUGIHARA—Electron Microsoopy of Ascites Cells
formed into an irregularly shaped profile, remark
able changes occur in the fine structure of the
cytoplasm. Numerous single, membrane-limited,
electron-lucent vesicles appear in a group in the
cytoplasm. The size of the vesicles varies, the
diameter being between 0.36 and 0.94 p. The
mitochondria are remarkably reduced in size. At
the same time, a great number of dense or less
dense, fine vesicles appear in the cytoplasm. It
is very interesting that numerous projections of
round, conical, or irregular shape are observed
at the peripheral part of the cytoplasm, being
surrounded by the cell membrane. That is, the
cytoplasm is divided into endo- and ectoplasm.
The former contains mitochondria and vesicles
of varying size, while the latter contains only
fine vesicles (Fig. 12).
The cytoplasmic projections are gradually isolat
ed from the cytoplasm, being predominantly round
in shape and surrounded with or without a delimit
ing surface membrane (Figs. 13 and 14). Concur
rently with these changes, the cell membrane dis
appears, and the ground substance of the cytoplasm
is destroyed into loss of its homogeneous appear
ance, showing irregular aggregations of osmiophilic
particles and formation of irregularly shaped gaps
without a limiting membrane. The isolated cyto
plasmic body is composed of fine, osmiophilic
particles homogeneously distributed or aggregated
into irregularly shaped masses of varying size
and outline, mitochondria without cristae, and
electron-lucent vacuoles (Figs. 13 and 14). The
osmiophilic particles are densely accumulated at
the nuclear membrane and in some areas in the
interior of the nucleus (Fig. 14). Occasionally
the nucleolus and the nucleolus-associated body
(10) are found attached to the nuclear membrane
(Fig. 13).
DISCUSSION
The electron micrographs obtained in the pres
ent study provide the first visual demonstration
of virus-like particles in nuclei of EAT cells,
which are of a great morphological similarity
to the particles enveloped by the smooth-surfaced
endoplasmic reticulum. Such particles have never
been observed in the nucleus (1, 3, 5, 6, 8, 9,
11, 12) or in the cytoplasm of YS cells (8).
However, the particles appearing in the cytoplasm
of YS cells are irregular in shape, size, and density,
and their source is less easily explained. There
is no morphological indication to imply the pres
ence of such particles in HCPA cells. The roughsurfaced endoplasmic reticulum has been found
in the EAT cell more abundantly than in the
YS and HCPA cells.
1169
Irregularly shaped bundles of coarse, dense fila
ments 25 m/i in diameter and 4 or 5 Min length
have been found in the cytoplasm of the Lücke
renal adenocarcinoma cell by Fawcett (2). The
fibrous elements observed in the YS cell in the
present study and by Wessel and Bernhard (8)
are smaller in width and less osmiophilic than
those in the Lückecell. It is possible that the
fibrous elements are elements of the disintegrated
mitochondria, because the mitochondria degener
ate to a nonhomogeneous mass which seems to
be a precursor of the fibrous elements. However,
the filaments of Lückecells have no relationship
to the mitochondria. The spindle-like body ap
pearing in the cytoplasm of YS cells may also
be related to the mitochondria, because it is sur
rounded with a few double membranes, each of
which has a great similarity to the limiting mem
brane of the mitochondria. However, no satisfac
tory explanation can be offered for the significance
of the fibrous elements and the spindle-like body.
Fibrous elements in YS cells have been observed
by Wessel and Bernhard (8), but the spindle-like
body has never been reported in light and electron
microscope observations.
Four electron micrographs of HCPA cells have
been presented to demonstrate remarkable changes
of the mitochondria in their form and structure.
The internal structure of the mitochondria is
less orderly than usual. They are of three or more
kinds that differ in size and internal structure.
Some mitochondria are swollen, and their center
is often free of ridges and is occupied by a matrix
of low density. The others decrease remarkably
in size but increase in number. Where there is
an increase in the quantity of vesicles or vacuoles,
there is a diminution in the mitochondria. This
fact has been interpreted as evidence of a relation
between the mitochondria and the accumulation
of vesicles or vacuoles. A peculiar picture has
been observed in the peripheral part of the cyto
plasm; it looks like the characteristic picture of
megakaryocyte found in guinea pig bone marrow
by Watanabe (7), because of division into the
endo- and ectoplasm. The present findings suggest
buddings-off from the cell surface. It is more
possible that the budding results from degenera
tive changes in cell organdÃ-es.As far as is known,
this is the first time a structure of exactly this
nature has come to attention in electron micros
copy.
SUMMARY
Ehrlich ascites tumor cells, Yoshida sarcoma
cells, and human cancerous peritonitis ascites cells
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1170
Cancer Research
were studied in thin sections with the electron
microscope.
All the Ehrlich ascites tumor cells examined
were found to contain virus-like particles of uni
form size and distinctive morphology in the endoplasmic reticulum in the cytoplasm and occasion
ally in the nucleus. The particles appearing in
the nucleus consist of hollow spheres (80-140
mpi) having a dense capsule about 12 m/* thick
and a dense inner body 40-70 nut in diameter.
Such particles have never been observed in Yoshida sarcoma cells and human cancerous peritonitis
ascites cells.
Parallel fibrous elements and occasional pecul
iar spindle-like bodies occur in the cytoplasm of
the Yoshida sarcoma cell. Their origin seems to
be related to the mitochondria, although their
significance remains obscure.
Division into endo- and ectoplasm occurs in
the human cancerous peritonitis ascites cells, sug
gesting a budding-off from the cell surface and
a fixation of some cells in degenerate condition.
REFERENCES
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Intracytoplasmic "Virus-like" Particles of Ehrlich Ascites
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M., and MOORE, D. H. Occurrence of
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WATANABE,Y. An Electron Microscopic Observation of
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nenmikroskopische Untersuchung von Ehrlich- und
Yoshida-Ascitestumorzellen. Ztschr. Krebsforsch., 62:14062, 1957.
YASÃœZÃœMI,
G., and HIGASHIZAWA,
S. Electron Microscope
Study of Sections of Ehrlich Mouse Ascites Tumors (First
Report). Gann, 47:527-28, 1956.
YASÃœZÃœMI,
G.; SAWADA,
T.; SUQIHARA,
R.; KIRIYAMA,M.;
and SUGIOKA,N. Electron Microscope Researches on the
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YASUZUMI,
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YOSHIDA,T. The Yoshida Sarcoma, an Ascites Tumor.
Gann, 40:1-21, 1949.
FIG. 1.—Ehrlich ascites tumor cell of 7 days' inoculation
age. The mitochondrion (if) is provided with the parallelarranged cristae, while the mitochondiia in the other part are
almost devoid of cristae and contain a matrix of low density
(MV) or an electron-lucent substance (V). The dense par
ticles (P) 55-75 m/i in diameter are found in the lumina of the
endoplasmic reticulum with smooth surface. The endoplasmic
reticulum (E) with the rough surface can be seen scattered
throughout all the area. Lipide droplets (L) in an irregular
shape are found attached closely to the Golgi complex (GC).
X 25,000.
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(1)
E ,
GC
GC
V
M V
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FIG. 2.—Ehrlich ascites tumor cell of 7 days' inoculation
age, showing the intracytoplasmic virus-like particles (P) in
the lumina of the smooth-surfaced endoplasmic reticulum near
the nucleus (Ar). At the point marked by A, the obliquely sec
tioned agranular portion of the membrane surrounding the
particle shows continuity with an adjacent granular portion,
which can definitely be identified as rough-surfaced endoplasniic reticulum. The dense particles (P) frequently demonstrate
a light core. Two ring structures (R) originated from the mito
chondria can be seen. (' marks an intranuclear canal. X 28,000.
FIG. 3.—Ehrlich ascites tumor cell at the same stage as
Figs. 1 and 2, showing a small group of virus-like particles (P).
Note the rough-surfaced endoplasmic reticulum (arrows) ap
pearing in circular or elongated profiles. R represents a ring
structure. Xao.OOO.
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FIG. 4.—Anarea of karyoplasm from an Ehrlich ascites tu
mor cell of 10 days' inoculation age, showing a deep indenta
tion at NM, virus-like particles (P), and a large intranuclear
vesicle (V). The virus-like particles (/J) are enclosed by a dense
membrane. The virus-like particle (I') can also he identified
within the inclusion of the vesicle (I'). The nucleus is enveloped
by the nuclear membrane (\M) with a double structure and
paekeil with highly differentiated chromosomal elements.
X 25,000.
FIG. 5.—AYoshida sarcoma cell, showing a portion of the
nucleus (.V) and a small region of the cytoplasm in which at
least five mitochondria can be seen. The mitochondrion
marked by ML is considerably swollen, but the enveloping
membrane is complete. The mitochondrion marked by an ar
row shows a clear, typical, internal structure, but its envelop
ing membrane is scarcely visible. J/N represents a degenerating
mitochondrion. Vesicles (!') of varying size and density appear
in the cytoplasm; some of them contain single (ON) or a fewgranules ((i} of different sizes. /•'
represents fibrous elements
near the nucleus (.V). X3(i,HOO.
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NM
..:
M
ML
M
M
V
V
V
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FIG. 6.—Yoshida sarcoma cell showing a portion of the
nucleus (.V) and a small region of the cytoplasm surrounded
by the mitochondria (M). A great number of vesicles of differ
ent sizes, being enveloped with single or double membrane
(DM), appear in the cytoplasm, which contain single grannie
(GS), a few smaller granules (G) or substance of low electron
density. The elongated, rough-surfaced endoplasmi? reticnlum
(E) can be seen at the left-hand upper corner. F represents
fibrous elements. X'27,600.
FIG. 7.—Yoshidasarcoma cell. Fibrous elements are clearly
visible at the point marked by F Mitochondria marked by M
represent degenerating stages /, shows a lipide droplet.
X27.500.
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V
V
v
GS
M
M
N
N
M
M
M
M
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FIG. 8.—Yoshida sarcoma cell. .SB marks a spindle-like
profile in a small size. The mitochondria (J/) are transparent,
being almost devoid of cristae. The rough-surfaced endoplasmic
reticulum (K) can seldom lie seen. L depicts a lipide droplet.
X46.000.
FIG. 9.—Yoshida sarcoma cell showing cross-section
through the spindle-like body (>Sß),
mitochondria (.I/), and
circular (CP) or elongated profiles (KP) with low density.
X 46,000.
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M
M
CP
SB
M
•¿EP
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FIG. 10.—Longitudinal section through tin- spindle-like
body (.S'fi.) appearing in a Yoshida sarcoma cell. The body is
composed of vesicles (I") of varying size which contain a homo
geneous mass of low density ora few granules (G). The body is
enveloped with a few lamellae, each of which consists of a
double membrane (arrows). Mitochondria
(.1/1 are swollen and
occasionally found along the spindle-like body. XHO.OOM.
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v
M
SB
M
V
G
M
M
V
»tx
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FIG. 11.—Human assîtes
cell of cancerous peritonitis, show
ing a round profile of the nucleus (.V) with an irregularly
shaped nucleolus (.VO), cytoplasm with shrunken'mitochon
dria (Mi, vaciiolizcd mitochondria (.1/1'), fine vesicles (I'), and
endoplasmi«'rcticiilinn (/•,').
X¿0,000.
FIG. li.—Human ascitcs cell of cancerous peritonitis, show
ing an irregularly shaped nucleus (.V) and the cytoplasm
packed with a great number of electron-lucent vesicles (!'"),
dense mitochondria (J/), and fine vesicles (/•'(')of different
densities and sizes. The pel ¡plieraiportion of the cytoplasm is
provided with numerous projections (PJ) of varying size and
shape. X 16,500.
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PJ
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FIG. 13.—Human aseites cell of cancerous peritonitis. A
portion of the nucleus (.V) with the nueleolua (A'O) and the
nucleolus-associated botl.v (\A) is demonstrated ¡itthe upper
side of the figure. The cytoplasm is filled with electron-lucent
vacuoles (V) of varying size, dense mitochondria (.I/), and fine
granules (G). Cellular projections (PJ) and bodies (IB) iso
lated from the cytoplasm can be seen at the periphery of the
cell. X 18,500.
FIG. 14.—Humanaseites cell of cancerous peritonitis, show
ing a degenerating stage of the cell. The nucleus shows the ir
regularly arranged chromosomal elements (CE) and osmiophilic particles (OP) densely accumulated at the periphery.
The nuclear membrane disappears at the point marked by the
arrow. The cytoplasm demonstrates irregularly shaped gaps
(OP), mitochondria (if) in vesicular shape, and isolated bodies
(IB). XI2,000.
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G
PJ
B
CF
P.
N
M
CR
B
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A Comparative Electron Microscopic Study on Ehrlich Ascites
Tumor Cells, Yoshida Sarcoma Cells, and Human Cancerous
Peritonitis Ascites Cells
G. Yasuzumi and R. Sugihara
Cancer Res 1958;18:1167-1170.
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