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Fine structure of the interstitial cells of leydig in the boar.

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Fine Structure of the Interstitial Cells of
Leydig in the Boar '
W. D. BELT AND L. F. CAVAZOS
Department of Anatomy, Tufts University School of Medicine,
Boston, Massachusetts
ABSTRACT
The interstitial cells of the testis of the boar have been characterized
by electron microscopy. The bulk of the cytoplasm, to one side of an eccentrically
placed nucleus, consisted predominately of a tightly packed agranular endoplasmic
reticulum in a system of anastomosing tubules. Free ribosomes and a few short strands
of granular endoplasmic reticulum were present only in a perinuclear or subplasmalemma1 location. Mitochondria were abundant as a cluster in the center of the cytosome. Surrounding them were dense bodies, most of which were bounded by a single
limiting membrane. The internum of the dense bodies exhibited a variety of appearances. Filaments of 70A were common but they were absent near the plasmalemma.
Between contiguous cells, irregularly disposed microvilli protruded into an intercellular
space of variable dimensions. Some sites of membrane fusion, resulting in maculae
occludentes, were observed between adjacent cells, while small desmosomes were
observed but rarely. Coated vesicles were frequent near to and continuous with the
plasmalemma as well as deeper within the cell, especially in association with elements
of the Golgi apparatus.
The fine structure of the normal interstitial cellZhas been described in several
species : human (Fawcett and Burgos, '56,
'SO), rat (Christensen, '59; Leeson, '63;
Schwartz and Merker, '65), opossum (Christensen and Fawcett, '61), rabbit (Crabo,
'63), mouse ( C a n and Carr, '62; Christensen and Fawcett, '66) and guinea pig
(Christensen, '65). Study of the fine structures of interstitial cells presents several
technical difficulties : (1) their sparse distribution in the testis of man and the usual
laboratory mammals, (2) the difficulties
attendant to cutting blocks of tissue, since
the lack of connective tissue results in
fraying of the tubules, and ( 3 ) difficulty
in preservation of the abundant and labile
agranular endoplasmic reticulum. The
problem of limited distribution was obviated by Christensen and Fawcett ('61) in
choosing the opossum, which has a profusion of interstitial cells, while in the guinea
pig, with many fewer interstitial cells,
Christensen ('65) was able to obtain coherent blocks and good preservation only
by perfusion of isolated testes with glutaraldehyde.
In search of a good species to serve as a
study model, we have turned to the boar.
The interstitial celIs of the boar were the
subject of early study by Ancel and Bouin
ANAT. REC., 158: 333-350.
('03) who also concluded that the interstitial cells, or interstitial gland of the
testis, as they termed it, were responsible
for the hormones which were needed for
the development of the secondary sex characteristics and sexual instincts. In a quantitative study, Bascom and Osterud ('27)
observed that the adult boar testis contained about 37% by volume of interstitial
cells. Also, according to our experience,
there is sufficient tenacity to the organ that
coherent blocks can be obtained - indeed,
the tissue is quite "tough."
MATERIALS AND METHODS
Material for this study was provided by
testes from one Duroc and one Landrace
boar ( S u s scrofa). Both testes were sampled from each animal. Blocks of tissue
were fixed in 1% and 2% osmium tetroxide in phosphate buffer (Millonig, 'Sl),
and processed into Epon 812 (Luft, '61).
Additional blocks were fixed in 3% glutaraldehyde in 0.1 molar phosphate buffer
(Sabatini, Bensch and Barrnett, '63; Sabatini, Miller and Barrnett, '64) and 6%
glutaraldehyde in s-collidine buffer (Ben-
333
334
W. D. BELT AND L. F. CAVAZOS
nett and Luft, '59). All fixatives were adjusted to pH 7.4-7.6 and used chilled for
2-3 hours. Blocks fixed in glutaraldehyde
were rinsed in cold buffer for 48 hours,
postfixed in osmium tetroxide for three
hours and processed into Epon 812. Thin
sections were stained in various ways prior
to examination. Most of the accompanying
illustrations are from material fixed in 6%
glutaraldehyde in s-collidine buffer, stained
with 5% uranyl acetate in 50% alcohol
followed by Reynolds ('63) lead citrate.
RESULTS
Interstitial cells of the mature boar were
present in magnificent profusion, totally
surrounding most seminiferous tubules. In
profile, these large cells, 20 to 30 CI in
length, showed a polygonal outline (fig. 1 ).
The nucleus was commonly displaced to
one side or corner of the cell with the remainder of the abundant cytoplasm containing mitochondria in the central portion
of the cytosome.
Most mitochondrial profiles were spherical with a diameter of 0.6-0.7 p, although
forms were observed from 0.3-1.0 p. Internally, they were characterized by a few
tubular internal membranes (figs. 2, 4),
with an occasional plate-like crista traversing the mitochondrion. The matrix was
notably dense in material fixed first in 6%
glutaraldehyde in collidine buffer. Following iixation in either 1% or 2% osmium
tetroxide, or in 3% glutaraldehyde in phosphate buffer, the mitochondria had a substantially less dense matrix, although it
was still moderately dense. Following all
fixatives used, dense mitochondrial granules were frequent within the matrix
(figs. 2,4).
The bulk of the cytoplasm consisted of
tubules of the agranular endoplasmic reticulum which were so abundant that there
was little between that could be termed
ground cytoplasm (figs. 1, 2, 3). Short
strands of granular endoplasmic reticulum
were observed (figs. 3, 5 ) , but they were
rare. Such rough-surfaced profiles were
usually restricted to a thin strip of cytoplasm either just inside the plasmalemma
or just outside the nuclear membrane. Sites
of continuity between the granular and
agrmular elements were commonly observed (fig. 5). Scattered rosettes of ribo-
somes were abundant in the same loci as
granular endoplasmic reticulum (fig. 5).
The precise fine structural configuration of
the agranular endoplasmic reticulum was
highly dependent on the fixative employed,
Of the two prime fixatives used, i.e., osmium tetroxide and glutaraldehyde, glutaraldehyde tended to preserve the agranular
endoplasmic reticulum in the form of tubules (figs. 1 , 2 , 3), while osmium tetroxide
as a prime fixative tended to preserve it in
the form of vesicles. Material which had
been fixed in 6% glutaraldehyde in collidine buffer showed the finest form of tubular structure, while that fixed in 3%
glutaraldehyde in phosphate buffer showed
an agranular endoplasmic reticulum which
was still tubular in form, the tubules of
which were decidedly larger than those
seen following 6% glutaraldehyde. However, even in the glutaraldehyde-fixed material some cells were observed which contained agranular endoplasmic reticulum
represented as large vacuoles. Conversely,
in the osmium-fixed material, occasional
small patchy areas of cytoplasm were observed in which fine tubular aggregates
were present amidst large vacuoles.
The Golgi apparatus consisted of flattened membranous saccules with the usual
associated small vesicles (fig. 4). Larger
vacuoles occurred often, but not regularly.
Apparently the Golgi apparatus can take a
highly disseminated form: in a single cell
several isolated portions of Golgi elements
were observed, sometimes even near the
celI periphery (fig. 1). It was a distinct
impression that the Golgi apparatus was
best developed in cells which had somewhat lesser quantities of agranular endoplasmic reticulum. Coated vesicles (fig. 4)
often were closely associated with the Golgi
saccules (vide infra). Some of the difficulty in identification of the Golgi apparatus i n cells with a large quantity of
agranular endoplasmic reticulum could
arise from the problem of distinguishing
one from the other; in some instances indications of membranous continuity between
the two occurred (fig. 4).
An abundance of dense bodies was present peripheral to the mitochondrial mass.
They were inconsistent as regards size,
number, and internal structure (figs. 1-5,
7). Most were between 0.5 CI and 1.0 P.
INTERSTITIAL CELLS O F THE BOAR
They were usually bounded by a single limiting membrane, except for some consisting entirely of dense membranous whirls
which did not appear to be totally membrane-limited (fig. 7). The latter were surrounded by agranular endoplasmic reticulum, oriented with respect to the dense
body, and often suggesting continuity. It is
perhaps pertinent that in interstitial cells
that are probably degenerating in the immature boar at six weeks of age (Cavazos
and Belt, '66), uncompacted whirls of
smooth agranular endoplasmic reticulum
may be encountered (fig. 6). Other dense
bodies may contain myelin figures, densely
granular material, crystal-like objects, and
arrays of dense tubules, singly or in combination. These varieties consistently possessed a limiting membrane.
Filaments of about 70 A were a frequent
cytoplasmic constituent, previously not reported for fully differentiated mammalian
interstitial cells (figs. 2 , 4). These were
most numerous near the nucleus in the
small strip of perinuclear ground cytoplasm, from which they coursed into the
adjacent cytosome. These filaments were
not observed in the peripheral strip of
ground cytoplasm, nor were they present
uniformly within the cytosome. They probably are present in all cells to some extent.
Often running side by side, they gave the
appearance in longitudinal section of microtubules, but in cross and oblique sections their solid filamentous nature was
indisputable (fig. 4).
Interstitial cells in the testis of the boar
were intimately related to each other in
their abundance. Contiguous cells were
separated by a space of varying dimensions. The gap space was 0.1 to 0.3 CI where
cells were closely packed. This space often
contained a flocculent material. Into it
protruded microvilli of variable length and
population density (figs. 1, 3, 5 ) . If the
Leydig cells were more widely separated,
bundles of collagenous fibers were often
present (figs. 2, 3). Small, poorly developed desmosomes were encountered
infrequently. More frequently, though still
not regularly, tight junctions were present
(figs. 1, 2 ) . In addition to microvilli, the
cell surface sometimes presented structures
resembling those which have been interpreted as pinocytotic folds by Fawcett '('65).
335
"Coated" vesicles were widely distributed.
They were seen in continuity with the
plasma membrane (fig. 1 ) and at various
levels of depth within the cell (fig. 5).
"Coated" vesicles were often seen in close
proximity to saccules of the Golgi apparatus with indications of membranous continuity between the two (fig. 4). There
were suggestions that these vesicles were
especially prominent at the surface of the
interstitial cell adjacent to the fine elements of the vascular system (figs. 8, 9).
DISCUSSION
Testicular interstitial cells of different
species possess a number of general features in common, but in detail a certain
amount of structural specificity prevails.
Most remarkable is the development of the
agranular endoplasmic reticulum. It is difficult to imagine how more agranular membranes could be so packaged. The species
most nearly similar in this regard is the
opossum (Christensen and Fawcett, '61 ),
with an agranular reticulum also represented as fine anastomotic tubules. The
normal human interstitial cell undoubtedly
has a significant quantity of this organelle
also (Fawcett and Burgos, '56, '60), as
judged by the number of vesicular structures representing it, but the precise form
is uncertain. A tubular system has been
observed in the interstitial cell of the human in testicular feminizing syndrome
(Gordon, Miller and Bensch, '64).
There seems little doubt that the most
consistent element of cells that secrete steroid is the abundance of agranular endoplasmic reticulum. The functional role of
the agranular reticulum has been well reviewed, generally (Jones and Fawcett, '66),
as well as specifically for the interstitial
cell (Christensen, ' 6 5 ) . Until relatively recently, this organelle was observed as vacuoles in all sites where it was notably developed, as for example in the adrenal
cortex (Zelander, '59; Lever, '55; Fujita,
'61; Yamori, Matsuura and Sakamoto, '61;
Sabatini and DeRobertis, '61; Sheridan and
Belt, '63) the interstitial cell (Fawcett and
Burgos, '56, ' 6 0 ) , and the corpus luteum
(Lever, '56; Yamada and Ishikawa, '60).
In relatively early studies, the sole demonstration of an extensively anastomotic system of agranular endoplasmic reticulum in
336
W. D. BELT AND L. F. CAVAZOS
a steroid secretory organ was in the fetal
human adrenal by Ross, Pappas, Lanman
and Lind (’58). After the emphasis made
by Ito (’61) on the tubular form of the
agranular endoplasmic reticulum in the
gastric parietal cell, the demonstration of
a tubular form in the opossum interstitial
cell (Christensen and Fawcett, ’61) and
the subsequent extensive display of the
system of fine anastomotic tubules in the
cells of the corpus luteum of the rat, armadillo and mink by Enders (’62), it has
become apparent that this membranous
tubular or occasionally cisternal system is
markedly labile, vesiculating with ease. In
this study, fixation by immersion resulted
in a tubular structure only following glutaraldehyde fixation.
The Golgi apparatus of the interstitial
cell of the boar occurs in a dispersed and
diffuse form. Most steroid secretory cells
are somewhat similar, with that organelle
less well developed than in cells synthesizing and secreting protein, where its function is relatively well characterized. The
frequent observation of “coated vesicles
(alveolate vesicles, acanthosomes, etc. ) in
close proximity to the Golgi apparatus, indeed, even in continuity with Golgi membranes, was similar to that of neurones
briefly reported by Palay (’63). He suggested that such structures might represent
“circulating plasmalemma.” Coated vesicles were also present close to or in continuity with the plasmalemma. In this location, such structures have been reported to
be involved in protein uptake in the
amoeba (Brandt and Pappas, ’60), insect
oocyte (Anderson, ’64; Roth and Porter,
’64) as well as in erythroblasts of mammals (Bessis and Breton-Gorius, ’59; Jones,
’65; Fawcett, ’64). The interstitial cell of
the boar may be a particularly favorable
site for further experimental characterization of this element.
The mitochondria in the interstitial cell
of the boar contain internal membranes
which are primarily tubular, in common
with most cells that elaborate a steroid secretory product (Belt and Pease, ’56). Only
here do mitochondria tend to localize in
the center of the cytosome. Since the mitochondria are somewhat more abundant
here than in other species, one might sus-
pect that energy requirements were higher,
but this is contradicted by the modest development of the membranous internum.
Pigment of one or several varieties
(Planel, Guilhem, Soleilhavoup and Tixador, ’64) is common in steroid secretory
cells. Most notable is the corpus luteum,
whose very name describes the abundant
pigmentation observed in many species.
Prior to fixation, the boar testes had a vivid
brick-red color. On this basis only, since
anciIlary procedures have not been carried
out, we assume that the dense bodies represent pigment, possibly a lipofuscin. Other
studies on boar interstitial cells report numerous PAS-positive granules (Cavazos
and Melampy, ’54). The dense bodies seen
in the present study differ from the pigment described in the guinea pig interstitial cell (Christensen, ’65) by being more
pleomorphic and in lacking the central
lipid droplet shown in the guinea pig, but
it must be remembered that the boar has a
paucity of lipid droplets in the interstitial
cells. The pigment may be formed from
focal areas of cytoplasmic degradation,
such as has been described in the liver
(Ashford and Porter, ’62; Hruban, Spargo,
Swift, Wissler and Kleinfeld, ’63) and seminal vesicle (Cavazos, Belt, Sheridan and
Feagans, ’64) among others. Since their
morphology in some instances resembled
‘‘residual bodies,” it would be pertinent to
consider aspects of relationship of these
dense bodies to lysosomes had the necessary histochemical and biochemical procedures been casried out to permit lysosomal
characterization.
While there are several characteristic
fine structural features of the interstitial
cells of the boar, i.e., filaments, paucity of
lipid droplets and abundant coated vesicles, most aspects are similar to those of
other species already described. A potential value of the boar testis is as a model
system for biochemical studies, for which
it seems well suited. One testis represents
an enormous volume of material. With its
abundance of interstitial cells, any homogenate of whole boar testis necessarily reflects a far greater proportion of interstitial
cell constituents than would a similar homogenate from the commonly used laboratory mammals.
INTERSTITIAL CELLS OF THE BOAR
ACKNOWLEDGMENT
The authors are grateful to Dr. R. M.
Melampy, Dr. L. L. Anderson, Dr. L. N.
Hazel and Mr. T. J. Morrissey, Iowa State
University, for their aid in procurement of
this material. Acknowledgment is made of
the technical assistance of Miss Shirley
Gray, Tufts University School of Medicine.
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Abbreviations
C, mitochondrial cristae
CF, collagen fibrils
CV, “coated vesicles”
DB, cytoplasmic dense bodies
EC, endothelial cell
F, cytoplasmic filaments
G, Golgi apparatus
GR, intramitochondrial granules
IC, interstitial cell
LF, longitudinally sectioned
cytoplasmic filaments
MO, macula occludens, “tight junction”
PC, perivascular cell
R, ribosomes
S, slit-like structures
T, tubular internal mitochondrial
membranes
TF, transversely sectioned
cytoplasmic filaments
W, whirls of agranular
endoplasmic reticulum
PLATE 1
EXPLANATION O F RIGURE
1 A large part of a n interstitial cell. The nucleus is eccentrically placed.
The mitochondria concentrate centrally, while dense bodies (DB) tend
to be located peripherally to the mitochondria. In this instance the
dense bodies are more numerous along the right edge. The Golgi
apparatus is diffuse, and with elements shown in three areas ( G ) .
Several slit-like structures ( S ) are present, which might represent a n
artifact. The remainder of the cytoplasm is filled with a tubular form
of agranular endoplasmic reticulum. A tight junction or macula
occludens (MO) is present between adjacent cells. A “coated vesicle”
is indicated at the arrow in continuity with the plasmalemma.
X 11,800
INTERSTITIAL CELLS OF THE BOAR
W. D. Belt and L. F. Cavazos
PLATE 1
339
PLATE 2
EXPLANATIQN OF FIGURE
2
340
The site of contact between two interstitial cells shows a n area of
membrane fusion, resulting in a macula occludens, the detailed
structure of which is seen as typically pentalaminar i n the photographically enlarged inset. The mitochondria shown in this field are
representative of those seen i n this study; they contain a relatively
dense matrix after 6% glutaraldehyde. Their internal membranes are
predominantly tubular ( T ) in character, although the occasional
partitions extending all or nearly all the way across the mitochondrion
are undoubtedly plate-like cristae ( C ) . Mitochondria1 granules (GR)
are common. Suggestions of cytoplasmic filaments (F) swirl through
the cytoplasm, although most of the cytosome between mitochondria
and dense bodies (DB) is filled with tubular elements of the agranular
endoplasmic reticulum. Cross section of collagenous fibrils (CF) are
seen intercellularly. X 31,000. Inset x 125,000.
INTERSTITIAL CELLS OF THE BOAR
W. D. Belt and L. F. Cavazos
PLATE 2
341
PLATE 3
EXPLANATION O F FIGURE
3
342
The plane of the section through this interstitial cell does not pass
through the bulk of the cytoplasm, but just through the perinuclear
cytoplasm that immediately surrounds the eccentrically placed nucleus. Although the cell does not have a base and an apex, it is as
though it were a horizontal section through the base of the cell a t
the level of the nucleus. Variously structured dense bodies are present,
some structured with membranous figures ( D B I ) and some homogeneously granular (DB2). The latter are not interpreted as lipid droplets because of their granularity and because they possess a limiting
membrane. Most of the ribosomes ( R ) are present as clusters of
polysomes just beneath the plasmalemma. A few strands of granular
endoplasmic reticulum are indicated by arrows. Note the profusion
of agranular endoplasmic reticulum i n all other areas of the cytosome. Microvilli are frequent but irregular a t the cell surface. Collagenous fibrils (CF) are present intercellularly. X 12,000.
INTERSTITIAL CELLS OF THE BOAR
W. D. Belt and L. F. Cavazos
PLATE 3
343
PLATE 4
EXPLANATION O F FIGURE
4 A portion of a Golgi apparatus ( G ) is shown with the ends of the
flattened saccules bearing dilations. “Coated vesicles” ( C V ) are Fresent with one in apparent continuity with Golgi membranes (arrow).
Cytoplasmic filaments are clearly present in both longitudinal ( L F )
and transverse (TF) section. X 56,000.
344
INTERSTITIAL CELLS OF THE BOAR
W. D. Belt and L. F. Cavazos
PLATE 4
345
PLATE 5
EXPLANATION OF FIGURES
5
Most commonly the junction of two contiguous cells demonstrates no
specialization of the cell surfaces other than a few stubby microvilli
extending into the small intercellular space. Ribosomes are limited to
a subplasmalemmal location ( R ) or (not shown) adjacent to the
nuclear membrane. Also present i n these locations are occasional
strands of granular endoplasmic reticulum. Continuity of the granular
and agranular endoplasrnic reticulum is indicated by the arrows.
“Coated vesicles” (CV) are frequently present just within the plasmalemma. x 65,800.
6
A portion of an interstitial cell of an immature boar shows whirls ( W )
of agranular endoplasmic reticulum which suggest a n early stage of
the membranous dense body encountered in the adult animal.
X 11,250.
7 Membranous dense bodies from adult animals do not appear to be
membrane limited, nor can the outer lamellae be distinguished with
certainty from oriented wrappings of agranular endoplasmic reticulum. x 46,000.
346
INTERSTITIAL CELLS OF THE BOAR
W. D. Belt and L. F. Cavazos
PLATE 5
347
PLATE 6
EXPLANATION OF FIGURES
348
8
An edge of a n interstitial cell ( I C ) adjacent to a capillary endothelial
cell ( E C ) with a n associated perivascular cell (PC). Numerous vesicular structures can be seen within the peripheral cytoplasm of all
three cell types. X 16,500.
9
Higher magnification of area delineated above. The vesicles in the
interstitial cell (IC) are doubly coated, with flocculent material on
the inner aspect of the vesicle and spiny protrusions from without,
while the vesicles within the perivascular cell ( P C ) only possess a
specialization on their internal aspect. x 83,000.
INTERSTITIAL CELLS OF THE BOAR
W. D. Belt and L. F. Cavazos
PLATE 6
349
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