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Special ultrastructural features of parathyroid cells from Swiss mice bearing Ehrlich's ascites tumor.

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Special Ultrastructural Features of Parathyroid Cells
from Swiss Mice Bearing Ehrlich's Ascites Tumor
JOHN S. LATTA AND TIMOTHY J. RUT2 2
Eppley Institute for Cancer Research and Department of Anatomy,
University of Nebraska College of Medicine, Omaha, Nebraska
As part of studies o n Ehrlich's ascites tumor cells transplanted into
ABSTRACT
Swiss mice some unique myeloid figures, were found with electron microscopy in
parathyroid cells, consisting of electron dense rings partially or completely encircling
the nuclei of many cells i n 7 of the 30 treated animals examined. These dense rings
were seen to be made up of tightly matted bands, which at free ends, spread out to
become continuous with agranular endoplasmic reticulum. The nuclei of these altered
cells were quite pleomorphic and were closer together than in normal tissue, indicating
decreased cell volume. Rough endoplasmic reticulum was scarce, mitochondria were
long and slender and free ribosomes were widely scattered in the cytoplasm. A possible
explanation for the development of these focal areas of degeneration is given.
As part of a study of transplanted
Ehrlich's ascites tumor, we became interested in notable ultrastructural changes
found in the cells of the parathyroid gland
which were apparently associated with
the marked debilitation resulting from the
rapid growth of the transplanted tumor.
These ultrastructural features have not
been demonstrated in previous studies of
the fine structure of normal parathyroids
in monkey (Trier, '58), rat (Davis and
Enders, '61; Lever, '58) and mouse (Hara
and Ishabashi, '64), or in normal or
adenomatous parathyroid of man or deer
(Roth and Munger, '62; Munger and Roth,
' 6 3 ) . Nor were these features observed in
parathyroids we prepared from numerous
untreated control mice.
MATERIALS AND METHODS
Thirty white, Swiss, female mice from 3
to 4 months old were injected intraperitoneally with 1 cm3of ascitic fluid containing approximately one million cells
which had been withdrawn from mice
bearing Ehrlichs ascites tumor. At intervals of from 15 to 21 days after injection,
the parathyroids were removed, fixed in
2% osmic acid, buffered with Millonig's
buffer, dehydrated in a graded series of
ethyl alcohol, transferred to propylene
oxide, and embedded in Epon 812. Sections were cut on a Porter-Blum MT-1
microtome and examined with a Philips
ANAT. REC.,160: 255-260
100 electron microscope. At sacrifice, all
mice were very debilitated and extremely
dehydrated.
RESULTS
Electron micrographs of parathyroids
from eight of the 30 treated mice showed
some very striking features. In all cells
of these eight cases, the cell volume was
considerably decreased so that the nuclei
were closer together and interdigitations
of the cell membranes less intricate than
in normal active cells. The nuclei were
quite pleornorphic with deep indentations
in the nuclear membranes, in contrast
with the more spherical, oval, or slightly
irregular form of typical nuclei of normal
cells. In the cytoplasm of cells from mo-st
animals of this tumor bearing group, very
little rough surfaced endoplasmic reticulum was found, compared with the abundant endoplasmic reticulum found in
untreated controls. However, free ribosomes were widely scattered throughout
the cytoplasm, with a tendency for their
segregation in certain areas, leaving other
areas entirely free. Numerous small vesicles from 50 to 60 mmH in diameter were
also widely scattered, often lined up
apparently having been derived from
typical lamellae of the Golgi apparatus.
1 This study was supported by U.S.P.H.S. training
grant 5Tl-GM 656-04.
2 U.S.P.H.S. Post Sophomore Medical Fellow, University of Nebraska College of Medicine.
255
256
JOHN S. LATTA A N D T I M O T H Y J. RUTZ
Some of these vesicles were larger and
more electron dense than others, apparently forming a graded series between them
and a few typical electron dense secretory
granules. The mitochondria in these cells
were long and slender, 300 mmw or less in
diameter (fig. l ) , as compared with those
in controls which were 400 mmw or less in
diameter.
The most striking feature found in the
parathyroids of this group of tumor bearing animals was a very electron dense ring
partially or completely surrounding the
nucleus in the majority of the cells (fig.
1). Under higher magnification, one could
see that these dense rings consisted of
wavy strands, usually quite tightly matted
together except at free ends where the
strands spread out and were apparently
continuous with endoplasmic reticulum
(fig. 2 ) . This continuity between endoplasmic reticulum and the matted filaments of the electron dense rings is well
shown in tangentially cut sections which
do not include the nucleus (fig. 3 ) .
Material from the treated animals which
did not show the electron dense rings
presented considerable variation. Some
parathyroid cells (15 days after inoculation) possessed a very abundant rough
endoplasmic reticulum interlaced with
large mitochondria and numerous Golgi
vesicles containing material of variable
electron density, including some typical
secretory granules indicative of a stimulating effect (fig. 4 ) . In a few instances,
we found closely packed strands, of endoplasmic reticulum adjacent to the nuclei
which were continuous with more loosely
arranged reticulum.
volume, the extreme nuclear pleomorphism, the reduction in number and size
of the mitochondria, and the compression
of the extensive modified endoplasmic
reticulum into partial or complete electron
dense rings. These dense rings are apparently lipoprotein in nature and represent
a degenerative phenomenon suggestive of
large myelin figures.
Very dense myeloid membranes have
been shown in injured cells of several
organs of rats surrounding sequestered
cytoplasmic areas undergoing focal degradation (Hruban, Spargo, Swift and
Wissler, '63). It has been suggested that
whorls of endoplasmic reticulum lose their
ribosomes, and the lipoprotein membranes
undergo further alteration, leading to the
appearance of very dense myeloid rings
(Fawcett, '61 ). The dense rings surrounding nuclei, as we have demonstrated in
parathyroid cells, are apparently formed
in this manner and are associated with a
degenerative process.
We are not aware that this arrangement
of myeloid figures has been previously
reported, at least in parathyroid cells. We
have studied the ultrastructure of parathyroid cells after experimental induction
of uremia and from pregnant and lactating
mice and found no such cytoplasmic
structures.
ACKNOWLEDGMENTS
The authors gratefully acknowledge the
assistance of Miss Rose Reynolds in preparation of the illustrations, and of Mr.
James Smith for the photographic work.
DISCUSSION
LITERATURE CITED
The above observations strongly suggest
that the experimentally introduced growing tumor has had an initial stimulating
effect on the parathyroid, shown by an
increase in rough endoplasmic reticulum
closely associated with enlarged mitochondria and very abundant Golgi vesicles
in varying stages of formation of secretory
granules. They further suggest that the
obvious tissue dehydration and other toxic
effects of the growing tumor were subsequently responsible for the decreased cell
Davis, R., and A. C. Enders 1961 Light and
electron microscopic studies on the parathyroid
gland. In: The parathyroids. Edited by R. 0.
Greep and R. V. Talmadge. C. C Thomas,
Springfield, Illinois.
Fawcett, D. W. 1961 The membranes of the
cytoplasm. Lab. Invest., 10: 1162-1178.
Hara, J., and I. Ishabashi 1964 Electron microscopic study of the parathyroid gland of the
mouse. Nagoya J. Med. Sci., 26: 119-124.
Holzmann, K., and R. Lange 1963 Zur Zytologie der GlanduIa parathyroiden des Menschen. Weitere Untersuchungen a n Epithelkorper - Adenom. Zeitschr. Zellforsch., 58: 759.
PARATHYROID ULTRASTRUCTURE IN TUMOR BEARING MICE
Hruban, Z., B. Spargo, H. Swift, R. W. Wissler
and R. G . Kleinfeld 1963 Focal cytoplasmic
degeneration. Am. J. Path., 42: 659-684.
Lever, J. D. 1958 Cytological appearances in
the normal and activated parathyroid of the
rat. A combined study of electron and light
microscopy with certain quantitative assessments. J. Endocr., 17: 210-217.
Munger, B. L., and S. I. Roth 1963 The cytology of the normal parathyroid gland of man
257
and the Virginia deer. A light and electron
microscopic study with evidence of secretory
activity. J. Cell Biol., 16: 379-400.
Roth, S. I., and B. L. Munger 1962 The cytology of adenomatous, atrophic and hyperplastic parathyroid glands of man. Arch. path.
Anat. Physiol., 335: 389-410.
Trier, J. S . 1958 The fine structure of the
parathyroid gland (Monkey). J. Biophys. and
Biochem. Cytol., 4: 13-22.
PLATE 1
E X P L A N A T I O N O F FIGURES
1 Parathyroid from a mouse 21 days after injection of ascitic fluid
containing Ehrlich’s ascites tumcr cells. Heavy electron dense rings
(DR) surrounded several very pleomorphic nuclei ( N ) . Mitochondria
( M ) are long and slender. NE-Neutrophilic leukocyte, E-Endothelium,
Nu-Nucleolus, PM-Plasma Membrane. Electron micrograph x 7030.
258
2
Portion of a parathyroid cell Prom the specimen illustrated in figure
1 under higher magnification to show the matted wavy strands
making up the dense ring. At the right, the dense mat frays out in
apparent continuity with modified endoplasmic reticulum. The condensation of nuclear chromatin ( N ) at the nuclear membrane is
suggestive of a degenerative process. Electron micrograph x 37,000.
3
Tangential section of a parathyroid cell from another mouse 21 days
after tumor inoculation. This continuity between this matted material
of the dense ring and modified endoplasmic reticulum (ER) is well
shown. A tangential section of a portion of the nuclear membrane
( N ) is illustrated. Electron micrograph X 10,300.
4
Apparent stimulation of parathyroid cells from a mouse 15 days after
tumor inoculation. Note the extensive granular endoplasmic reticulum (GER), the nearly spherical nuclei, and the various stages i n
density of vasicular contents leading to typical secretion granules
(SC). Electron micrograph X 10,300.
PARATHYROID ULTRASTRUCTURE IN TUMOR BEARING MICE
John S. Latta and Timothy J. Rutz
PLATE 1
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