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Embryologic origin of the various epithelial cell types in the second kind of thyroid follicle in the C3H mouse.

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Embryologic Origin of the Various Epithelial Cell Types
in the Second Kind of Thyroid Follicle
in the C3H Mouse1
SEYMOUR H. WOLLMAN AND S. ROBERT HILFER
Laboratory of Molecular Biology, NCI, NIH, Bethesda, Maryland 20014, and
Department ofBiology, Temple Uniuersity, Philadelphia, Pennsylvania 19122
ABSTRACT
The thyroid gland of the C3H mouse is composed largely of the
usual follicle but i t also contains a second kind of follicle. To ascertain the embryologic origin of the cell types in each of these follicles, ventral pharyngeal
outpocketings and ultimobranchial outpocketings were isolated (before they
fused to form the thyroid gland) from the 12-day-old fetus of the C3H mouse. The
outpocketings were implanted into different kidney capsules of adult C3H mice
and were allowed to grow for several months. Transplants were then excised and
examined by electron microscopy.
The ventral contribution formed large aggregates of follicles and was recognized as a distinct bump on the surface of the kidney. It formed only typical
thyroid epithelium arranged in follicles containing colloid. On the other hand,
the ultimobranchial contribution usually formed only a small number of follicles, generally of small size. It was readily located because the follicles occurred
next to a white plaque of bone or cartilage a t the site of implantation. The ultimobranchial contribution formed follicles containing four cell types: a ciliated
cell, a cell with abundant agranular reticulum, a cell with many free ribosomes
and fiber and occasional hemidesmosomes, and the C cell which was the most frequent cell type. No typical thyroid epithelium was observed in the ultimobranchial transplant.
These observations suggest that the C cell in the usual follicle is derived from
the ultimobranchial contribution, and that the second kind of follicle is largely
an ultimobranchial contribution but the typical thyroid epithelium in i t is
largely or entirely a ventral contribution.
A second kind of follicle occurs in the
thyroid gland of the C3H mouse (Dunn, '44;
Gorbman, '47; Wetzel and Wollman, '69; Wollman and Neve, '71). In addition to typical
thyroid epithelial cells it was found to contain
ciliated cells, AR cells (with an abundance of
agranular reticulum), C cells (Wetzel and
Wollman, '69; Wollman and Neve, '71) and U
cells (Neve and Wollman, '72) (a usually
stratified squamous epithelial cell in which
the basal cells have hemidesmosomes). Although i t has been suggested with some evidence that the cells of this second kind of follicle are of ultimobranchial origin (Gorbman,
'471, no experimental study as yet has shown
that this is the case. It appears likely, however, t h a t some of these cells, such as the
ciliated cell, the C cell and the U cell, are of
ANAT. REC.
(1978)191: 111-122.
ultimobranchial origin since they occur in
transplants to the kidney capsule of embryonic ultimobranchial outpocketings of the rat
(Wollman and Hilfer, '77). In reference to the
origin of the C cell we mean to imply only that
C cells enter the thyroid with the ultimobranchial body. I t is clear from the work of
LeDouarin and LeLievre, ('70) that C cells are
originally derived from the neural crest but
are found in the ultimobranchial body in adult
birds.
In this paper we report an attempt to clarify
the origin of various cell types in the second
kind of follicle in the thyroid gland of C3H
mice.
Received Aug. 1, '77. Accepted Oct. 31, '77.
' Presented in brief at the Seventh International Thyroid Conference in Boston, Massachusetts in June, 1975.
111
112
SEYMOUR H. WOLLMAN AND S. ROBERT HILFER
MATERIALS AND METHODS
Ventral thyroid rudiments (fig. 1)and ultimobranchial outpocketings (fig. 2) were obtained (before they fused) from 12-day-old
fetuses of C3H/HeN mice. They were implanted separately into the kidney capsule of
adult C3H mice fed Purina Laboratory Chow.
Some months later the mice were killed by
exsanguination after they were lightly a n esthetized with ether, and kidneys were examined for the transplants. Ventral thyroid rudiments were recognized as well-defined lumps
on the surface of the kidney. Ultimobranchial
outpocketings were invariably found next to a
white plaque of cartilage and, occasionally,
bone on the surface of the kidney. The transplant was excised and fixed for examination
by electron microscopy by immersion in a 2.5%
solution of glutaraldehyde (Ladd) in 0.1 M
cacadylate buffer, pH 7.3 at room temperature
for one hour followed by one hour in 1.0%OsO,
in the same buffer. Tissues were dehydrated in
a graded series of ethanols, propylene oxide
and embedded in Epon 812. Thick sections
Fig. 1 Excised ventral pharyngeal outpocketing prior
to transplanting to kidney capsule. Note epithelium partially covered by mesenchyme. X 125.
Fig. 2 Excised ultimobranchial outpocketings. Note
epithelium with lumen (arrow) partially covered by mesenchyme. x 125.
were stained with toluidine blue and thin sections with uranyl acetate and lead citrate.
Sections of transplants of nine ultimobranchial outpocketings and of five ventral outpocketings were examined.
RESULTS
The transplant of the ventral thyroid rudiment to the kidney capsule gave rise to a large
aggregate of the usual thyroid follicles with
densely stained colloid differing from follicles
in situ primarily in the absence of C cells. The
individual cells had a n ultrastructural morphology similar to the typical thyroid epithelial cell in t h e thyroid in situ (fig. 3).
The transplant of the ultimobranchial outpocketings gave rise to from one to four follicles. The follicular epithelium consisted of a
single or, in places, a double layer of cells
which surrounded a lumen containing a heterogeneous material. The four cell types t h a t
were found in this follicle resembled, in general, those occurring in the second kind of
thyroid follicle (figs. 7, 8). These were:
a. Ciliated cells. These cells occurred singly
or in clusters and usually but not always
touched the basal lamina (figs. 4, 5).
b. C cells (figs. 5, 6). These cells were
wedged between ciliated cells (fig. 5) or AR
cells (fig. 6);they touched the basal lamina
but usually did not touch the lumen of the follicle. They differed from C cells in the thyroid
gland in situ primarily in displaying a much
higher incidence of desmosomes (fig. 6). In
addition, in a few cases a C cell was found in
contact with the lumen of the follicle (fig. 6).
c. AR cells, (figs. 7-91. These cells were generally large and dense. They contained a variable abundance of agranular reticulum and
occasionally some secretory vesicles (fig. 8).
They touched the lumen and usually touched
the basal lamina.
d. Cells resembling U cells (figs. 10-13) but
possessing a much lower incidence of hemidesmosomes. Most profiles showed none (fig.
10). These cells frequently lay in between the
base of a ciliated cell or a n AR cell and the basal lamina (not illustrated), but sometimes
touched the lumen (fig. 10, 11, 13). Evidences
of differentiation into stratified squamous
epithelium were lacking.
The lumen of this follicle contained a
heterogenous colloid and cell debris, the most
readily recognized being of ciliated cells.
No typical thyroid epithelial cells were
found in this follicle. However, in one trans-
ULTIMOBRANCHlAL ORIGIN OF SOME THYROID CELLS
plant of an ultimobranchial outpocketing
three follicles that could not be distinguished
from the usual thyroid follicle were found in
addition to the second kind of follicle. I t is
likely that this was a case in which development had progressed further than recognized
and in which a small number of cells from the
ventral contribution had reached the ultimobranchial outpocketing and were transplanted with it.
DISCUSSION
It is clear that with the exception of the
typical thyroid epithelial cell all the cell types
commonly observed in the second kind of
thyroid follicle are found in the follicles derived from the transplant of the ultimobranchial outpocketings into the kidney capsule. The general absence of typical thyroid
epithelial cells from this transplant suggests
that the typical cells in the second kind of follicle are derived from the ventral pharyngeal
contribution of the embryo to the thyroid
gland.
Although the cells present in the transplant
resemble those in the second kind of follicle,
there are some differences: for example, the
small number of C cells that touch the lumen
apparently have not been observed to occur in
any kind of follicle in the C3H mouse or rat
(Stux et al., ’61; Young and Leblond, ’63). C
cells touching a lumen apparently have been
observed in the dog thyroid (Teitelbaum e t al.,
’701, and the authors reporting this observation point out that it was a purely ultimobranchial follicle as was the case in the present observations.
Second, the U cells seem to differ somewhat
from U cells in the thyroid gland in the
marked decrease in abundance of hemidesmosomes and in the lack of typical maturation
into stratified squamous epithelium although
this lack sometimes occurs in the thyroid in
situ in the adult mouse.
113
There is a surprising difference between
mouse and rat in the characteristics of the follicles developing in the transplants of ultimobranchial outpocketings to the kidney capsule. In the rat, C cells and U cells are in different follicles in the transplant and in the
thyroid in situ (Wollman and Hilfer, ‘77). In
the mouse all cell types (including C cells and
U cells but excepting the typical thyroid epithelial cell) are together in one type of follicle
in the transplant. The reason for this difference is unknown.
ACKNOWLEDGMENTS
We are grateful to Delta Uphoff for the
timed pregnant female C3H mice and to
Franklin E. Reed for expert technical assistance.
LITERATURE CITED
Dunn, T. B. 1944 Ciliated cells of the thyroid of the
mouse. J. Nat. Cancer Inst., 4: 555.
Gorbman, A. 1947 Functional and morphological properties in the thyroid gland, ultimobranchial body, and persisting ductus pharyngiobranchialis IV of a n adult
mouse. Anat. Rec., 98: 93-101.
LeDouarin, N., and C. LeLievre 1970 Demonstration de
l’origine neurale des cellules a calcitonine du corps ultimobranchial chez I’embryon de poulet. CR. Acad. Sc.
(Paris), 270: 2857-2860.
Neve, P., and S. H. Wollman 1972 Fine structure of a fifth
type of epithelial cell in the thyroid gland of the C3H
mouse. Anat. Rec., 172: 37-43.
Stux, M., B. Thompson, H. Isler and C. P. Leblond 1961 The
“light cells” of the thyroid gland in the rat. Endocrinology, 68: 292-308.
Teitelbaum, S.L., K. E. Moore and W. Shieber 1970 C cell
follicles in the dog thyroid: demonstration by in uiuo perfusion. Anat. Rec., 168: 69-78.
Wetzel, B. K.,and S. H. Wollman 1969 Fine structure of a
second kind of thyroid follicle in the C3H mouse. Endocrinology, 84: 563-578.
Wollman, S. H., and S. R. Hilfer 1977 Embryologic origin of
various epithelial cell types in t h e thyroid gland of the
rat. Anat. Rec., 189: 467-478.
Wollman, S.H., and P. Neve 1971 Ultimobranchial follicles
in the thyroid glands of rats and mice. Recent Progress in
Hormone Research 27: 213-234.
Young, B. A,, and C. P. Leblond 1963 The light cells are
compared to the follicular cells in the thyroid gland in the
rat. Endocrinology, 73: 669-686.
PLATE 1
EXPLANATION OF FIGURES
3 Ultrastructural appearance of a representative cell from transplant of ventral outpocketing to kidney capsule four months after implantation. Note abundance of short
microvilli entering lumen a t top of figure, of apically located lysosomes (L)and of the
rough endoplasmic reticulum (R) characteristic of the typical thyroid epithelial cell.
X 9,700.
4
114
Apical portion of a ciliated cell found in follicle in transplant of ultimobranchial outpocketing into kidney capsule four months after implantation. Note basal bodies (B)
and cilia (C) a t top of figure, relatively widely spaced cisternae of rough endoplasmic
reticulum (R)and polysomes (P) characteristic of ciliated cells in the second kind of
thyroid follicle in the C,H mouse. N, nucleus X 17,500.
ULTIMOBRANCHIAL ORIGIN OF SOME THYROID CELLS
PLATE 1
Seymour H . Wollman and S. Robert Hilfer
115
PLATE 2
EXPLANATION OF FIGURES
Figs. 5, 6 C cells in follicle in transplant of ultimobranchial outpocketing to kidney
capsule four months after implantation.
5 Portions of two C cells containing a n abundance of secretory granules (SG);neither
touches the lumen. One lies under a ciliated cell with basal bodies (B) in evidence,
very long microvilli (arrow) and a Golgi zone (GI apical to the nucleus, the other under a bit of a n AR cell. X 10,100.
6 The apical portion of a C cell with characteristic secretion granules (SG).This cell is
unusual in having a desmosome (D) between it and the neighboring AR cell and particularly because i t appears to make contact with the lumen of the follicle (arrow).
X 15,300.
116
ULTIMOBRANCHIAL ORIGIN OF SOME THYROID CELLS
Seymour H. Wollman and S. Robert Hilfer
PLATE 2
117
PLATE 3
EXPLANATION OF FIGURES
Figs. 7-9 AR cells in a follicle from a transplant of an ultimobranchial outpocketing
into kidney capsule four months after implantation. The amount of agranular reticulum
in these cells varies from a great deal in figure 7 to almost none in figure 9. The cells
show short, stubby microvilli and rounded mitochondria (MI.
Figures 8 and 9 have an apical set of flat, closely spaced cisternae of rough endoplasmic reticulum (R). Figure 8 has
three secretory vesicles (SV)also seen with considerable frequency in t h e AR cell in the
second kind of thyroid follicle in the mouse. L, lumen. Figure 7 X 8,400, figure 8
X 12,000, figure 9 X 25,000.
118
ULTIMOBRANCHIAL ORIGIN OF SOME THYROID CELLS
Seymour H Wollrnan and S. Robert Hilfer
PLATE 3
119
PLATE 4
EXPLANATION OF FIGURES
Figs. 10-13 Possible examples of U cells in follicles found in transplants of ultimobranchial outpocketings to the kidney capsule four months after implantation. These
cells were in contact with both lumen (L) and basal lamina and contained a n abundance
of microfilamentous material in clusters (F). There was a high frequency of microvesicles, possibly pinocytotic (P), a t the basal end of the cell. M, mitochondria.
10 Flat U cell touching lumen and basal lamina. The cells contained fibrillar material
and polysomes but no hemidesmosomes. X 19,900.
11 Detail from the left end of figure 10.
12 U cell with hemidesmosomes (arrow).
X
X
30,000
19,000,
13 Apical cytoplasm from a cuboidal cell with the general cytoplasmic characteristics of
a U cell. No hemidesmosomes were found on this cell. X 29.000.
120
ULTIMOBRANCHIAL ORIGIN OF SOME THYROID CELLS
Seymour H. Wollman and S. Robert Hilfer
PLATE 4
121
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embryology, second, epithelium, kinds, c3h, mouse, origin, typed, thyroid, follicle, cells, various
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