[CANCER RESEARCH 38, 3164-3173, October 1978]
0008-5472/78/0038-0000$02.00
Structure of Normal Testis and Testicular Tumors in Cyprinids
from Lake Ontario1
John F. Leatherland-
and R. A. Sonstegard3
Departments of Zoology ¡J.F. L.¡and Microbiology ¡R.A. S.¡.College of Biological Science, University of Guelph, Guelph, Ontario, Canada NIG 2W1
ABSTRACT
RESULTS
Two types of testicular tumor were evident in cyprinid
fishes collected from Lake Ontario. Both types of tumors
appeared to be of Sertoli cell origin. One contained pre
dominantly Sertoli cells with little or no lipid content and
germinal cells in only small numbers. The second con
tained large numbers of spermatogonia
together with
Sertoli cells that contained large amounts of lipid and
smooth endoplasmic reticulum. Small, apparently inactive
Leydig cells were present in both types of tumors and
also in testes of fish not bearing gonadal tumors.
Structure of the Nontumorous Testis. There is some
controversy regarding the description of the testis in tele-
INTRODUCTION
Lake Ontario carp (Cyprinus carpio), goldfish (Carassius
auratus), and their F, hybrids suffer epizootics of gonadal
tumors that may be environmentally
induced (20, 21). This
report describes the structure and ultrastructure of 2 types
of testicular tumors in carp and goldfish hybrids and the
testis in normal cyprinids
in order to characterize
the
predominant cell types composing the tumors.
MATERIALS
AND METHODS
Collection and Maintenance of Fish. Fish were captured
by netting from Hamilton Harbour, Lake Ontario, Canada,
in late summer and returned to Guelph for biopsy. Samples
of testicular tumor tissue were taken from 10 hybrids.
Samples of apparently normal testis were taken from 2
hybrids and 6 goldfish. A piece of each tissue was fixed in
Bouin's fluid and embedded in Paraplast for routine histological examination, and other pieces of suitable size were
fixed in 5% cacodylate-buffered
(pH 7.5) glutaraldehyde for
2 hr, washed overnight in cacodylate buffer (with 8% su
crose added, pH 7.4), postfixed for 2 hr in cacodylatebuffered (pH 7.4) 1% OsO4, and embedded in Epon. Sec
tions of paraffin-embedded
tissues were made at Setting 7
and stained with periodic acid-Schiff or hematoxylin and
eosin. Survey sections of Epon-embedded
tissue were
made at 0.5 to 1.0 and stained at 70°with azure II for
examination
by light microscope.
Ultrathin sections of
Epon-embedded
material were mounted on uncoated cop
per grids, stained with uranyl acetate and lead citrate, and
examined by means of a Philips 200 electron microscope.
1 Supported by grants from the National Cancer Institute of Canada,
Environment Canada, and the National Research Council of Canada.
' To whom requests for reprints should be addressed.
1 Research Scholar, National Cancer Institute of Canada. Present address:
Department of Biology and Pathology, McMaster University, Hamilton,
Ontario, Canada.
Received August 18, 1977; accepted June 20, 1978.
3164
osts. Some authors distinguish
between the lobular testis
in fish and the tubular testis of mammals [see review by
Grier and Linton (8)]. In cyprinid fishes the testis is made up
of lobules (Figs. 1 and 2) similar to those described in other
species of fish (1, 2, 9); the component cells in teleosts
appear to be homologous to those found in mammals. The
lobules are formed by a boundary layer of "lobule boundary
cells" (7-9), which are Sertoli cell homologs and germ cells.
In the reproductively
nonfunctional
fish used in this study,
the germ cells were predominantly
spermatocytes and cells
that we identify as spermatogonia,
although other stages of
spermatogenesis
were present (Figs. 1 to 4). The sperma
tocytes and germ cells in later stages of spermatogenesis
were found in clumps while the cells that we identify as
spermatogonia
were most commonly
present as solitary
cells (Figs. 1 and 2). The latter were large cells with deeply
invaginated nuclei and prominent nucleoli. They contained
numerous mitochondria,
many of which were closely asso
ciated with granules of an electron-dense
amorphous ma
terial (Fig. 3) similar in appearance to the nuages or chromatoid bodies described in mammals (4, 5, 18). In addition
the cytoplasm contained
numerous free ribosomes and
small numbers of membrane-bound
granules (Fig. 3) and
extensive Golgi profiles (Fig. 4). The spermatocytes
were
commonly attached to each other by tight junctions; these
took the form of closely applied dense membranes but
lacked desmosomal characteristics.
They had more or less
spherical nuclei and fewer mitochondria
than did the sper
matogonia. A small number of electron-dense granules with
their accompanying
mitochondria
were also evident in
these cells.
The Sertoli cells were situated around the periphery of
the seminiferous
lobules, where they were in contact with
the basement membrane (Figs. 4 to 7). Cytoplasmic exten
sions of some Sertoli cells extended between the germinal
cells and other cells and were in contact with the lumen of
the seminiferous tubule (Figs. 2, 5, 6, 8, and 9). Adjacent
Sertoli cells were joined by junctional complexes (Fig. 9)
composed of regions similar to tight junctions, intermediate
gap junctions, and desmosomes found in many epithelial
tissues (6). Adjacent Sertoli and germ cells appeared to be
joined by junctions similar to those evident between adja
cent germ cells (Fig. 7). The Sertoli cells contained large,
deeply invaginated
nuclei with prominent nucleoli; only
small numbers of mitochondria were found in them. Sertoli
cells were also marked by their content of large cytoplasmic
lipid droplets (Figs. 2, 5, 6, 8, and 9). The cytoplasm also
contained moderate amounts of smooth endoplasmic reticCANCER
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Testicular Tumors in Lake Ontario Cyprinid Fish
ulum (Figs. 5 and 7), some of which encircled the lipid
droplets (Figs. 5, 6, and 8). Electron-dense lysosome-like
organelles were evident in a small proportion of cells. Areas
of Sertoli cell cytoplasm adjacent to the basilar membrane
commonly contained small vesicles that were either taking
material from, or secreting material into, the basal lamina
(Fig. 7). Some of the Sertoli cells in contact with the
seminiferous tubule lumen appeared to release lipid into
the lumen (Fig. 5) while others appeared to form close
contacts with sperm in the lumen (Fig. 8).
Leydig cells were found in relatively small numbers be
tween the seminiferous tubules (Figs. 7 and 10). They were
small cells with irregularly shaped nuclei. Their cytoplasm
contained numerous mitochondria and abundant smooth
endoplasmic reticulum. Some Leydig cells were character
ized by a marked electron density of the cytoplasm and
nucleus. Lipid droplets were only rarely found.
Structure of Testicular Neoplasms. Two types of tumors
were identified, both of which appeared to be proliferations
of the epithelial rather than interstitial tissue. For the
purpose of the descriptions given here, they will be consid
ered as separate types of neoplasm, although they may well
be variants of a single type.
In the first type (tumor type I) (Figs. 11 to 15), the cells
were spindle shaped with deeply invaginated nuclei. The
cells formed close contacts with the basal lamina and
appeared to be joined together by extensive complexes of
desmosomes (Figs. 13 and 15). Some of these cells con
tained pronounced whorls of smooth endoplasmic reticu
lum (Fig. 14) that in a small number of cells were associated
with lipid droplet inclusions. There were apparently no
germ cells within the tumor tissue, nor was there a clearly
perceptible formation of seminiferous lobules. Only a few
Leydig cells were found (Fig. 15).
In the second tumor type (type II) (Figs. 16 to 19), most of
the cells were interpreted as large spermatogonia similar to
comparable cells in the testes of fish without tumors (Fig.
19). Interspersed with the spermatogonia were cells that
resembled the Sertoli cells in the fish without tumors. They
contained marked accumulations of lipid droplets often
associated with whorls of smooth endoplasmic reticulum
(Figs. 18 and 19). These Sertoli cells formed close contacts
with the basal lamina and appeared to be actively involved
in pinocytosis (exo or endo) at the region of interface with
the membrane (Fig. 18). Leydig cells were few in number
but, where present, were essentially similar in appearance
to cells in fish without tumors (Fig. 18).
DISCUSSION
The Sertoli cells in the testes of non-tumor-bearing fish
constitute the epithelium of the seminiferous lobules. Basally, they are in contact with the basal lamina, while apically
they extend to the lumen of the tubule. They are character
ized by their cytoplasmic content of lipid droplets. The
description of these cells given here is similar to that given
for those of goldfish (2), guppy (1, 8), and northern pike (9).
The role of Sertoli cells in gametogenesis and spermiogenesis is still not clear, even in mammals (6). In mammals
they appear to have the necessary organelles for steroidogenesis, and Fawcett (6) proposed that they may produce
OCTOBER
local accumulations of steroid material that are required for
normal development of the maturing germ cells. Very little
is known of Sertoli cell function in lower vertebrates. In
some fish that develop spermatogenic cysts, the epithelial
cells lining the cysts have been termed Sertoli (1, 7, 15) but
it is far from clear whether these are homologous with the
so-called Sertoli cells in other teleosts examined (2). Billard
ef a/. (2) questioned the use of the term Sertoli cell to
describe these cells in several teleosts, since they were
unable to ascertain functional homologies with Sertoli cells
of the mammalian testis. Nor were they able to find smooth
endoplasmic reticulum in these cells; thus, they could not
ascribe to them a steroidogenic function. In this study the
Sertoli cells were found to contain moderate amounts of
smooth endoplasmic reticulum, providing some evidence
for steroidogenesis within these cells. Moreover, the appar
ent liberation of lipid into the seminiferous tubule lumen,
also shown by Billard ef a/. (2) in rainbow trout, and the
close associations between sperm in the lumen and Sertoli
cell cytoplasm suggests that the Sertoli cells may play a
role in the process of sperm maturation. The deep penetra
tion of sperm heads into Sertoli cells, so characteristic of
the mammalian testis (6, 17), was not found. While no
evidence of phagocytosis by Sertoli cells was found in these
studies, it has been reported in other species of teleost (8,
9).
The movement of materials from the basal lamina into
Sertoli cells (or in the reverse direction) has been well
documented in mammalian species (6). Similar pinocytotic
profiles were evident in the nonneoplastic Sertoli cells
studies here.
The cells we classify as spermatogonia were characteris
tically large cells containing relatively electron-lucent nu
clei, prominent nucleoli, and electron-dense cytoplasmic
granules associated with groups of mitochondria (Fig. 3).
These electron-dense granules resemble the nuages or
chromatoid bodies found in mammalian spermatogonia,
spermatocytes, oogonia, and oocytes (4, 51, 18). These
large, solitary cells situated close to the basal area of the
seminiferous epithelium in cyprinids have been called sper
matogonia, since they resemble the descriptions of this cell
type in other fish species (1, 2, 9). However, since the
prominent nuages in mammals are more characteristically
found in spermatocytes (4, 5, 18), it is possible that these
putative spermatogonia have been incorrectly identified in
the few fish species thus far examined by means of electron
microscopy. The putative spermatogonia in the gonadally
dysgenetic fish used here have many of the characteristics
of gonocytes found in the mammalian testis neonatally (23).
Thus, the putative spermatogonia may, in fact, be homolo
gous to the gonocytes or prespermatogonial cells. Descrip
tions of spermatogonia similar to those made here were
given by Billard ef al. (2) for goldfish and by Grier (8) and
Grier and Linton (9) for guppies and northern pike, respec
tively. These cells and spermatocytes formed characteristic
junctional complexes with each other and with adjacent
Sertoli cells. The junctional complexes took the form of
parallel electron-dense areas along segments of adjacent
plasma membranes, separated by a moderately electrondense intercellular space. The junctions were somewhat
similar to those found in rat (11) but lacked the complex
1978
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3165
J. F. Leather/and
and R. A. Sonstegard
ridge-like structure present in mice (16, 18); desmosomes
with associated microfilaments were found only between
adjacent Sertoli cells.
Leydig cells were present in only small numbers in the
normal testes. They were small angular cells, rich in mito
chondria and containing large amounts of smooth endoplasmic reticulum but only small amounts of lipid material.
They resembled inactive Leydig cells in tetrapods (3, 12,
19). The small size of the cells and their relatively small
number probably reflect the gonadally dysgenetic state of
the fish used in this study.
The 2 types of tumors reported here may well represent
different types of Sertoli cell proliferation. In both types the
lobular structure of normal testis was lacking, but one of
the prominent elements in both tumor types was a cell that
contained lipid droplets and associated whorls of smooth
endoplasmic reticulum. The second tumor type may not be
a purely Sertoli cell neoplasm, since the predominating
cells appear to be spermatogonia (or gonocytes). There is a
strong possibility that both tumor variants can be classed
as gonadoblastomas. In humans, gonadoblastomas are
composed of mixtures of proliferating germ cells and Sertoli cells (14) and occur almost exclusively in subjects who
have underlying gonadal dysfunction.
In type II tumors the lipid-containing cells were intermin
gled with putative spermatogonia (gonocytes). In-the type I
tumors, lipid-containing cells were rarely found but, when
present, were identical with the lipid cells of the type II
tumor. Many cells in the type I tumors, although lacking in
lipid droplets, had well-developed whorls of smooth endo
plasmic reticulum. All the cells in the type I tumors were
characterized by a profusion of desmosomal complexes. In
nonneoplastic testicular tissue, desmosomes were evident
only between adjacent Sertoli cells, providing further, al
though weak, evidence that the neoplastic cells are of
Sertoli cell origin.
In both variants of the tumor there was no evidence of
Leydig cell proliferation. Indeed, there appeared to be fewer
Leydig cells in all parts of the testes of tumor-bearing fish
than in those of fish without tumors. This appears consist
ent with the finding of low plasma testosterone levels in
tumor-bearing cyprinids (J. Sumpter, J. F. Leatherland, and
R. A. Sonstegard, unpublished data).
In the nonneoplastic portions of the testes of hosts
bearing either of the tumor variants, gametogenesis was
reduced as compared with that in fish without tumors.
Some spermatogonial tissue was evident in the neoplastic
tissue in both tumor types. In teleosts the gametes are
produced under the influence of androgenic hormones
secreted by Leydig cells (13, 15, 22). The poor gamete
production possibly reflects a low androgen production by
the Leydig cells. Conversely, it may indicate an interference
in the role played by Sertoli cells on gamete production and
maturation. In mammals the Sertoli cells are thought to
secrete steroids (6), and in Sertoli cell tumors in mammals
the cells appear to secrete estrogenic steroids (10). It is
possible that the poor gametogenesis in the tumor-bearing
fish is caused by elevated estrogen production by the
proliferating Sertoli cells, which inhibits normal spermiogenesis. There is some evidence to support the possibility
of a secretion of estrogen by the neoplastic tissue. Foci of
3166
ovum development were commonly found adjacent to tu
mor tissue, suggesting that material secreted by the tumors
was capable of eliciting a localized conversion of testicular
to ovarian tissue. Another possibility is that the presence of
the ovotestis indicates primary gonadal dysgenesis, predis
posing the gonad to tumor development.
ACKNOWLEDGMENTS
We wish to thank L. Lin and B. Hicks for their technical help.
REFERENCES
1. Billard, R. La Spermatogenèse de Poecilia reticulata. III. Ultrastructure
des Cellules de Sertoli. Ann. Biol. Animale Biochim. Biophys., 10: 2750,1970.
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Poissons Téleostéens.
I. ÉtudeUltrastructurale. Ann. Biol. Animale
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3. Christensen, A. K. Leydig Cells. In: D. W. Hamilton and R. 0. Greep
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4. Eddy. E. M. Fine Structural Observations on the Form and Distribution
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7. Gresik, E. W.. Quirk, J. G., and Hamilton, J. B. Fine Structure of the
Sertoli Cell of the Testis of the Teleost Oryzias latipes. Gen. Comp
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8. Grier, H. J. Aspects of Germinal Cyst and Sperm Development in Poecilia
latipinna (Teleostei: Poeciliidae). J. Morphol., 146: 229-250, 1975.
9. Grier, H. J., and Linton, J. R. Ultrastructural Identification of the Sertoli
Cell in the Testis of the Northern Pike. Esox lucius. Am. J. Anat., 149:
283-288, 1977.
10. Huggins, C., and Moulder, P. V. Estrogen Production by Sertoli Cell
Tumours of the Testes. Cancer Res.. 5: 510-514,1945.
11. Kaya, M., and Harrison, R. G. The Ultrastructural Relationship between
Sertoli Cells and Spermatogenic Cells in the Rat. J. Anat., 121: 279-290.
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12. Lam, F., and Farner, D. S. The Ultrastructure of the Cells of Leydig in
the White-Crowned Sparrow (Zonotrichia leucophrys gambelii) in Rela
tion to Plasma Levels of Luteinizing Hormone and Testosterone. Cell
Tissue Res., 769. 93-109. 1976.
13. Lofts, B., Pickford, G. E., and Atz, J. W. Effects of Methyl Testosterone
on the Testes of a Hypophysectomized Cyrpinodont Fish, Fundulus
heteroclitus. Gen. Comp. Endocrinol., 7: 74-88. 1966.
14. Mostofi, F. K., and Price, E. B. Tumors of the Male Genital System. Atlas
of Tumor Pathology, Fascicle 8. pp. 310. Washington, D. C.: Armed
Forces Institute of Pathology, 1973.
15. Pandey, S. Effects of Hypophysectomy on the Testis and Secondary Sex
Characters of the Adult Guppy, Poecilia reticulata Peters. Can. J. Zool..
47: 775-781, 1969.
16. Ross, M. H. The Sertoli Cell Junctional Specialization during Spermiogenesis and at Spermiation. Anat. Record. 186: 79-104, 1976.
17. Ross, M. H., and Dobler, J. The Sertoli Cell Junctional Specializations
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18. Russell, L., and Frank, B. Ultrastructural Characterization of Nuages in
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20 Sonstegard. R. A. Environmental Carcinoenesis Studies of Fishes of the
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Testicular Tumors in Lake Ontario Cyprinid Fish
Fig. 1. Testis in nontumorous goldfish. A paraffin-embedded preparation showing the lobular nature of tissue. Arrowheads, putative spermatogonia. H&E.
x 400.
Fig. 2. Epon-embedded preparation of testis in nontumorous goldfish showing putative spermatogonia (large arrowheads) and small, lipid-filled Sertoli
cells (small arrowheads). Azure II, x 400.
Fig. 3. Putative spermatogonium in a nontumorous goldfish. Note the invaginated nucleus and electron-dense cytoplasmic droplets encompassed by
mitochondria, x 18,600.
Fig. 4 Putative spermatogonium in a nontumorous goldfish. Note how it is separated from direct contact with the basal lamina (arrowheads) by part of a
Sertoli cell (S). Note also the cell junctions between the Sertoli cell and spermatogonia. x 10,800.
Fig. 5. Sertoli cells (S) in adjacent seminiferous tubules in a nontumorous goldfish. Note the abundant smooth endoplasmic reticulum in the cytoplasm
and large lipid droplets. Note also the apparent release of lipid into the lumen of the seminiferous tubule. Sc, spermatocyte. x 16,350.
Fig. 6. Part of a Sertoli cell adjacent to the basal lamina (arrowheads) and lumen of the seminiferous tubule in a nontumorous goldfish. Note the fusion of
lipid droplets, x 23.650.
Fig. 7. Leydig cells (L) in a nontumorous goldfish separated from a Sertoli cell (S) by the basal lamina. The 2 cells are separated by a moderately electrondense basal lamina. Note the pinocytotic activity (arrowheads) of the Sertoli cell, x 10,800.
Fig. 8. Sertoli cell adjacent to the lumen in a nontumorous goldfish. Note the close association between a sperm head (Sp) and a lipid droplet of the
Sertoli cell, but note also that there is no penetration of the sperm head into the Sertoli cell cytoplasm, x 27.880.
Fig. 9. Junctional complex between adjacent Sertoli cells adjacent to the seminiferous tubule in a nontumorous goldfish. Note the close association of
sperm head (arrowhead) with one of the Sertoli cells, x 25.920.
Fig. 10. Leydig cells adjacent to a blood capillary in a nontumorous goldfish. Note the cytoplasmic vesicles (arrows), the abundant smooth endoplasmic
reticulum, and the small number of cytoplasmic inclusions in the Leydig cells, x 16,930.
Figs. 11 and 12. Tissue from tumor type I in paraffin-embedded H&E-stained (Fig. 11) and Epon-embedded. azure ll-stained preparations (Fig. 12). Note
the spindle-shaped cells, the absence of the normal lobular arrangement, and poor differentiation of the component cells of the testis. x 395.
Fig. 13. Group of cells in a type I tumor showing the prolific complexes of desmosomes. One cell has whorls of smooth endoplasmic reticulum
(arrowhead), x 11,135.
Fig. 14. Presumptive Sertoli cell in a type I tumor showing the whorls of smooth endoplasmic reticulum surrounding lipid droplets, x 19.420.
Fig. 15. Leydig cells (L) in a type I tumor. Note the enlarged basal lamina compared with the nontumorous condition. S. presumptive Sertoli cells, x
11.500.
Figs 16 and 17. Tissue from tumor type II in paraffin-embedded, H&E-stained (Fig. 16) and Epon-embedded, azure ll-stained preparations (Fig. 17). The
predominant cells are putative spermatogonia and smaller numbers of lipid-filled Sertoli cells only evident in the Epon-embedded preparation (arrowheads),
x 395.
Fig. 18. Leydig cells (L) and Sertoli cells (S) in a type II tumor. Note the pinocytotic activity at the basal lamina and the whorls of smooth endoplasmic
reticulum associated with lipid droplets in the Sertoli cells, x 11,390.
Fig. 19. The 2 predominant cell types in a type II tumor, presumptive spermatogonia (Sg) and lipid-filled Sertoli cells (S), x 6,860.
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Testicular Tumors in Lake Ontario Cyprinid Fish
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VOL. 38
Testicular
Tumors in Lake Ontario Cyprinid
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Testicular Tumors in Lake Ontario Cyprinid Fish
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3173
Structure of Normal Testis and Testicular Tumors in Cyprinids
from Lake Ontario
John F. Leatherland and R. A. Sonstegard
Cancer Res 1978;38:3164-3173.
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