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Uptake of radioiodine in follicles of dog C-cell complexes studied by autoradiograph and immunoperoxidase staining.

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THE ANATOMICAL RECORD 200:461-470 (1981)
Uptake of Radioiodine in Follicles of Dog C-Cell
Complexes Studied by Autoradiograph and
lmmunoperoxidase Staining
YOKO KAMEDA, KAZUO IKEDA, AND AKIRA IKEDA
Department ofAnatomy, Kawasaki Medical School, Kurashiki City, O k a y a m , 701 -01
Japan
ABSTRACT
C-cell complexes are special cell groups consisting of a mass of
C-cells associated with other epithelial elements and cysts. They are remnants
of ultimobranchial bodies retaining fetal characteristics. In the C-cell complexes
there are follicular cells in various stages of differentiation, i.e., the cell clusters
not yet organized into follicles, primordial follicles with small lumens and comparatively enlarged follicles storing plentiful amounts of colloid. They have a
morphology similar to follicular cells of fetal thyroid glands and react to antiserum
to 19s thyroglobulin. In order to determine whether or not the follicles in these
complexes have the ability to incorporate radioiodine, autoradiography after a
single injection of '''I was combined with immunoperoxidase staining using specific anti-calcitonin, anti-C-thyroglobulin, and anti-19s thyroglobulin antisera.
The 19s-positive cells not yet organized into follicles did not take up radioiodine.
Primordial follicles showed a heavy accumulation of silver grains over their follicular lumens storing new 1 9 s thyroglobulin as colloid. Comparatively enlarged
follicles revealed a strong autoradiographic reaction and their labeling patterns
were identical with those of typical thyroid follicles. These results confirm that
the follicles in C-cell complexes, as well as thyroid follicles, can incorporate radioiodine and are related to thyroid hormone synthesis. That is, functional thyroid
follicles can arise from the ultimobranchial bodies.
In the thyroid gland of dogs there are C-cell
complexes, special cell groups of C-cells (Kameda, 1971, 1976). They are remnants of ultimobranchial bodies and retain a n abundance
of fetal characteristics for a very long time,
showing a large number of undifferentiated
cells and immature C-cells even in adult dogs
(Kameda e t al., 1980; Kameda and Ikeda,
1980a). The complexes are composed of C-cells
in various stages of differentiation, undifferentiated epithelial cells, and cysts of various
sizes. In addition, many complexes contain colloid-containing small follicles similar in light
and electron microscopic features to those of
the definite thyroid gland that have developed
from the midventral evagination of the pharynx (Kameda, 1971, 1973, 1977). The undifferentiated cells, which are peculiar embryonic
cells, are characterized by a small amount of
cytoplasm, a chromatin-dense nucleus, and a
lack of immunoreactivity for antisera (Kameda, 1973; Kameda et al., 1980). The cells
are more numerous in younger animals and,
in fetal dogs, they occupy the greatest part of
the complex. In a previous developmental and
immunohistochemical study (Kameda et al.,
1980), it was evidenced that the undifferentiated cells can, over an extended period of
time, develop into clusters of follicular epithelial cells which proceed to form lumens and
develop into structurally differentiated follicles. That is, not only C-cells but also follicular
cells can differentiate from cells of ultimobranchial body origin.
In contrast to thyroid follicular cells, the
cells derived from ultimobranchial bodies develop very slowly; cell clusters not yet organized into follicles and primordial follicles with
small lumens are recognizable even in the complexes of adult dogs (Kameda and Ikeda,
1980a). The clusters of follicular cells as well
as the follicles that develop from them in the
complexes can be stained immunocytochemically with antiserum against 19s thyroglob-
0003-276X/81/2004-0461$03.00
0 1981 ALAN R. LISS, INC.
Received Odober 23, 1980;accepted January 8,1981.
462
Y. KAMEDA, K. IKEDA, AND A. IKEDA
ulin (Kameda, 1977; Kameda et al., 1980; Kameda and Ikeda, 1980a). The presence of this
particular glycoprotein is essential for the formation of thyroid hormones. The anti-19s thyroglobulin antiserum does, however, crossreact with inactive precursors and polymers of
19s thyroglobulin and further with the glycoprotein existing in thyroidal cysts. Therefore, positive immunocytochemical staining is
not conclusive proof of the presence of 19s thyroglobulin and of thyroid hormone secretion.
In order to determine whether the follicular
cells derived from the ultimobranchial bodies
possess the ability to synthesize and secrete
thyroid hormones, the present study investigates by light microscopic autoradiography
whether or not the follicles in complexes can
incorporate lZ5I.The serial sections are also
treated for distinct identification of constituent
elements of complexes with immunoperoxidase method using specific anti-calcitonin,
anti-C-thyroglobulin (C-Tg),and anti-19s thyroglobulin antisera, respectively.
C-Tg is the largest molecular weight component (mol wt approx. 2,600,000) of thyroglobulin, which is composed of several components (Kameda and Ikeda, 1979b). Antiserum
to C-Tg reacts to secretory granules of C-cells
in addition to follicular cells and follicular colloid. The relationship between calcitonin and
C-Tg has been described in the previous studies: (1)C-Tg and calcitonin antisera cross-react
to a certain degree (Kameda and Ikeda, 1979b);
2) the reaction of anti-C-Tg antiserum in fetal
C-cells appears at earlier stages and more
strongly than that of anti-calcitonin antiserum
(Kameda et al., 1980); 3) tumour cells in medullary thyroid carcinoma, a distinct neoplasm
derived from C-cells, reveal a far stronger immunoreaction for C-Tg than for calcitonin
(Kameda et al., 1979).These data strongly suggest that the C-Tg molecule contains the specific peptide chain composition corresponding
to the biosynthetic precursor of calcitonin. Furthermore, the biochemical nature of C-Tg in
comparison with that of other thyroglobulin
Fig. 1. Serial sections of C-cell complexes of a dog 8 hours
after injection of Na1151(100 p,Ci/kg). Thyroid parenchyma
in upper portion. F, follicles in thyroid; C, cyst in complex.
x 100. a. Immunoperoxidase reaction for calcitonin. A
greater portion of the complexes are occupied by C-cells in
various stages of differentiation. Insertion: Higher magnification ( x 520)of the complex. The C-cells vary in size and
in their immunoreactivity to anti-calcitonin antiserum.
Undifferentiated cells (arrow) showing no immunoreaction
are also observable. b. Immunoperoxidase reaction for 19s
components has been reported in detail in
other papers (Kameda, 1981a,b).
MATERIALS AND METHODS
Twelve young dogs of either sex, weighing
1t o 4 kg, were given a single intraperitoneal
injection of 100 pCi carrier-free Na'251 (The
Radiochemical Centre, Amersham, England)
per kg body weight. The animals were killed
1,5,8,24,and 48 hours after the injection. The
thyroid glands were fixed in Bouin's solution
for 24-48 hours. The specimens were embedded in paraffin and cut into 5-7-pm-thick longitudinal total serial sections.
Some sections were stained with hematoxylin-eosin or periodic acid-Schiff (PAS). For
immunological staining, an unlabeled antibody-enzyme bridge technique was used as
previously described (Kameda and Ikeda,
1978). Three specific antisera were employed:
anti-porcine calcitonin antiserum, anti-dog CTg antiserum, and anti-dog 19s thyroglobulin
antiserum. The preparation and serological
studies of these antisera have been described
previously (Kameda and Ikeda, 1979a,b). The
sections were reacted with the following sequence of solutions after hydration with phosphate-buffered saline (PBS): an appropriate
dilution of the primary antisera (anti-calcitonin, anti-C-Tg, and anti-19s antisera) for 5
hours, goat anti-rabbit globulin antiserum
( 1 : l O ) for 15 minutes, and rabbit anti-peroxidase antiserum (1:lO) for 15 minutes. After
incubation in horseradish peroxidase solution
(0.5 mg/100 ml) containing 0.1%bovine serum
albumin, reaction products were developed
with 3,3'-diaminobenzidine tetrahydrochloride (0.5 mg/ml) and HzO2(0.01%).Sections
were washed three times for 7 minutes each
with PBS between the steps. All reactions were
carried out a t room temperature. Control reactions included replacing the primary antisera with normal (nonimmune) rabbit serum
and absorbing primary antisera with excess of
the respective antigens (extracted porcine calcitonin, dog C-Tg, and dog 19s thyroglobulin).
thyroglobulin. No immunoreactive cells are detectable in
complexes. Follicular cells in thyroid parenchyma reveal
intense immunoreactivityand foamy substances in cyst are
also reactive. c. Autoradiographic reaction and poststaining
with hematoxylin-eosin. The follicular colloid in thyroid
parenchyma shows an accumulation of silver grains. The
smaller follicles reveal denser autoradiographic images.
There are essentially no grains over the complexes.The cyst
is devoid of silver grains.
E9P
464
Y. KAMEDA, K. IKEDA, AND A. IKEDA
Figure 2 a-c.
DOG C-CELL COMPLEX FOLLICLE '%I UPTAKE
465
Fig. 2. A C-cell complex containing clusters of follicular
cells 8 hours after injection of Nalz5I. Figures a to c are
serial sections of the complex stained by three different
methods. a. Immunoperoxidase reaction for calcitonin. The
immunoreactivity of C-cells in complex is weaker than that
of the cells in thyroid parenchyma. x 115. b. Immunoperoxidase reaction for 19s thyroglobulin. Small clusters of
19s-positive cells are distributed in the complex. Small follicles (F) in upper left. x 115. c. Autoradiographic reaction
and poststaining with hematoxylin-eosin. Silver grains are
localized over follicular lumens (F) at upper left, whereas
not present over C-cell masses and over clusters of follicular
cells (arrows). x 115.d. Higher magnification of the complex
in b. The follicular cells are loaded with numerous reaction
products for 19s thyroglobulin but not yet organized into
follicles. x 580. e. Higher magnification of the complex in
c. The clusters of follicular cells reveal more concentrated
nuclei and smaller cytoplasm than C-cell masses. A small
follicle (arrow) forming among follicular cells shows a distinct accumulation of silver grains, whereas the silver
grains over the clusters of follicular cells and C-cells do not
exceed those of the background. x 580.
For autoradiography, the sections were
coated with an aqueous dilution of melted Sakura NR-M2, dried, and stored in lighttight
boxes containing Silica Gel. After 2- to 4-week
exposure a t 4"C, radioautography was developed for 5 minutes in Konidol X, fixed in Fuji
Super Fix, and stained with hematoxylineosin.
cells revealed variable amounts of reaction
products for calcitonin and C-Tg, representing
various stages of differentiation (Fig. la). Mature C-cells with extensive cytoplasm were
filled with numerous immunoreactive secretory granules. Immature C-cells contained
sparse reaction products in the still-small
amount of cytoplasm. The undifferentiated
cells displayed scanty cytoplasm and chromatin-dense nuclei, and were more numerous in
the complexes of younger animals. They were
not stained with any antisera. In this type of
complex, there were no cells showing the immunoreactivity for 1 9 sthyroglobulin (Fig. lb).
The distribution of silver grains was not observed in the complexes (Fig. lc). That is, neither C-cells nor undifferentiated cells possessed the ability to concentrate radioiodine.
Subsequently, the second type of complex
was investigated. As the most immature form,
there were complexes containing primitive follicular cells not yet organized into follicles
RESULTS
Eight out of the twelve dogs given a single
injection of Na'251had one or more C-cell complexes. Two types of C-cell complexes were observed as described previously (Kameda, 1971;
Kameda and Ikeda, 1980a).In one type of complex there were a large number of C-cells a t
various developmental stages, undifferentiated cells, and various-sized cysts. A second
type contained follicular cells in addition to
these elements.
When the first type of complex was stained
with anti-calcitonin and anti-C-Tg antisera, C-
466
Y.KAMEDA, K. IKEDA, AND A. IKEDA
Fig. 3. Autoradiograph of a C-cell complex containing primordial follicles and small follicles (Ff24 hours after injection
of NalZ5I.Poststained with hematoxylin-eosin. Heavy accumulation of silver grains is obsemed over follicular lumens.
x 230.
(Fig. 2). The cells had a small amount of cytoplasm and chromatin-dense nuclei (Fig. Be).
Although they were indistinguishable from
undifferentiated cells with hematoxylin-eosin
staining, their cytoplasm was filled with numerous reaction products after immunoperoxidase staining using slightly diluted anti-19s
antiserum (Fig. 2b,d). The 19s-positive cells
were arranged in small cell clusters and dispersed among C-cell masses in the complexes.
(Fig. 2a,b). No significant incorporation of radioiodine into the 19s-positive cells was observed (Fig. 2c,e).
In the complexes containing primordial follicles which represented small cavities storing
new colloid, the follicles revealed a dense immunoreaction for 1 9 s thyroglobulin. Especially, colloid in follicular lumens was stained
densely with all dilutions of anti-19s antiserum up to the marginal dilution. Heavy accumulation of silver grains was observed over
the follicular colloid (Fig. 3); the labeling was
correlated with the intensity of immunoperoxidase reaction. Autoradiographic reaction was
specific for the follicular colloid.
In the complexes containing comparatively
enlarged follicles which were lined with a
number of follicular cells and stored a plentiful
amount of colloid in the follicular lumens, the
follicles revealed the same immunoperoxidase
and autoradiographic reactions as typical thyroid follicles (Fig. 4). The autoradiographic reaction of dog thyroid glands has been reported
in the previous study (Kameda, 1981b). In complexes as well as in thyroids, the follicular cells
were stained diffusely with slightly diluted
anti-19s antiserum and colloid was stained
more densely with the highly diluted antiserum (Fig. 4b). Homogeneous accumulation
of silver grains was obtained over the follicular
lumens (Fig. 4c). Among these, usually,
smaller follicles accumulated more numerous
Fig. 4. Serial sections of a C-cell complex containing
comparatively enlarged follicles 24 hours after injection of
NalZ5I.Congestion (arrows) which reveals a n excessive accumulation of blood owing to dilation of blood capillaries is
seen in masses of C-cells. F, follicles. x 150. a. Immunoperoxidase reaction for C-Tg. Secretory granules of C-cells
show strong immunoreaction. Using anti-C-Tg antiserum
absorbed previously with a small quantity of 19s thyroglobulin, the reaction of colloid is denser than that of follicular cells. b. Immunoperoxidase reaction for 19s thyroglobd i n . Using the slightly diluted antiserum, the reaction of
follicular cells is conspicuous. c. Autoradiographic reaction
and poststaining with hematoxylin-eosin. Follicular colloid
shows a heavy accumulation of silver grains.
DOG C-CELL COMPLEX FOLLICLE 1251 UPTAKE
467
468
Y.KAMEDA, K. IKEDA, AND A. IKEDA
silver grains. Ring reactions, i.e., relatively
dark images in the shape of a ring over the
peripheral region of the colloid, were observed
over many lumens. The intensity of autoradiographic images increased with time and
reached a peak a t 24 hours after the injection
of 1251.At 48 hours after the injection, the intensity of reaction was similar to that after 24
hours. Thus, the follicles in complexes possessed the ability to accumulate radioiodine
and the labeling pattern was identical with
that of thyroid follicles. In this type of complex,
most of C-cells were similar to ordinary thyroid
C-cells, i.e., mature (Fig. 4a). They contained
numerous reaction products for calcitonin and
C-Tg in extensive cytoplasm. The C-cells revealed no autoradiographic reaction (Fig. 4c).
DISCUSSION
It is generally accepted by recent researchers
that follicular cells and C-cells of thyroid
glands are two distinct cell lines with different
origins; i.e., follicular cells are derived from
midline outpouching of the ventral pharyngeal
floor and C-cells from the ultimobranchial bodies. However, we confirmed in a series of studies on C-cell complexes, remnants of ultimobranchial bodies, that the follicular cells are
derived not only from the median thyroid primordium but also from the ultimobranchial
bodies; i.e., the follicular cells as well as C-cells
develop from undifferentiated cells within the
complexes (Kameda et al., 1980; Kameda and
Ikeda, 1980a,b). Transitional features of undifferentiated cells changing into primitive follicular cells were found in the C-cell complexes
by immunoperoxidase and electron microscopic observations (Kameda, 1973; Kameda
et al., 1980). Furthermore, follicular cells in
various developmental stages are detectable
in the complexes: 19s-positive cell clusters not
yet organized into follicles,primordial follicles,
and comparatively enlarged follicles. With the
exception of maturing late, the follicular cells
derived from ultimobranchial bodies represent
the same characteristics as the cells from median thyroid primordium; both cells display the
same light and electron microscopic features
(Kameda, 1971,1973,1976)and are controlled
by the pituitary gland (Kameda, 1974): Furthermore, they reveal the immunoreaction for
19s thyroglobulin (Kameda, 1977).
Thyroglobulin is heterogeneous. In addition
to the main protein component, 19s thyroglobulin, there are several components with
slower and faster sedimentation coefficients.
The slower components, 3-8S, 12s and 17-18S,
are subunit precursors or noniodinated forms
of 19s molecule. They are formed in rough endoplasmic reticulum and Golgi complexes of
follicular cells (Nadler et al., 1964; Whur et
al., 1969). Iodination of thyroglobulin takes
place in the follicular lumens adjacent to the
plasma membrane, resulting in a 19s molecule. The iodinated 19s molecules are accumulated in follicular lumens as colloid. The
faster components, 27S, 32S, 37s and >37S,
are usually accepted as polymers of 19s molecule (Salvatore et al., 1965; Van der Walt and
Van Jaarsveld, 1972). They are formed by random noncovalent aggregation of 19s molecules
during storage in follicular colloid (Frati et al.,
1974).
It is well known by biochemical experiments
using sucrose density gradient ultracentrifugation that radioactive iodine is predominantly accumulated in 19s component fraction
at all time intervals after injection and that
its accumulation in faster and slower component fractions is very low (Robbinset al., 1966;
Roche et al., 1968). The incorporation of radioiodine into each thyroglobulin component
could be determined more accurately by the
use of 2-16% polyacrylamide gradient gel electrophoresis after dogs were injected with
Na'251 (Kameda, 1981b). When the distribution of radioactivity in each thyroglobulin component was determined along the gels, more
than 90%of total thyroid radioiodine was observed in the 19s component band, and 27S,
32S, and 12s component bands also revealed
weak radioactivities. No radioactivity was observed in the other component bands. Similarly, when the incorporation was determined
by the gel autoradiography, a markedly strong
autoradiographic reaction was obtained over
19s component band and the reaction conspicuously increased with time. The 27S, 32S, and
12s components also revealed weak autoradiographic reactions but little increase of the
reaction with time. Thus, radioactive iodine is
specifically incorporated into the 19s component; i.e., iodination, production of thyroid hormones (thyroxine and triiodothyronine), is specific for 19s component.
In spite of being in various stages of maturation and having different functions, the antigenicity of each thyroglobulin component is
very similar; the slower and faster components
have an antigenic determinant in common
with 19s component (Kameda and Ikeda, 1978,
1979a). The antisera to slower and faster components, as well as antiserum to 19s component, react to both follicular cells and luminal
DOG C-CELL COMPLEX FOLLICLE 1251 UPTAKE
colloid after immunoperoxidase staining.
Therefore, it is impossible to determine by immunohistochemical methods alone whether or
not the follicular cells derived from ultimobranchial bodies produce 19s component and
are related to thyroid hormone synthesis. Autoradiographic technique is necessary to clarify this problem. The present light microscopic
autoradiography clearly demonstrated that
the follicles in complexes as well as thyroid
follicles revealed a n accumulation of silver
grains after dogs were injected with NalZ5I.
The accumulation conspicuously increased
with time and so-called ring reactions were
observed over the peripheral region of follicular colloid. That is, the follicles in complexes
possess the ability to accumulate radioiodine
and their labeling pattern is identical with
that of thyroid follicles. It is clear that the follicular cells in complexes produce 19s component to secrete thyroid hormones; the follicular cells derived from ultimobranchial bodies
have a function completely identical with the
cells from median thyroid primordium.
The follicular cells derived from ultimobranchial bodies develop very slowly. In respect to
immunoreaction and folliculogenesis, the follicular cells in complexes coincide with the
cells of fetal thyroid glands (Kameda, 1973,
1977; Kameda et al., 1980; Kameda and Ikeda,
1980a). The present study further confirmed
that their ability to incorporate lZ5Iwas also
similar to that of fetal thyroid follicles described in rabbits and human (Olin et al., 1970;
Roques et al., 1972). That is, in complexes the
follicular cells remaining as cell clusters still
lacked the ability to incorporate radioiodine.
The iodine accumulation began synchronously
with the formation of follicles; the onset of lZ5I
collection and storage coincided with the appearance of the first follicles. The primordial
follicles forming among cell clusters revealed
a markedly heavy accumulation of silver
grains. Along with the enlargement of follicular lumens, their autoradiographic images
became similar to those of thyroid follicles of
postnatal dogs.
In complexes as well as in thyroids, silver
grains were specifically located on follicular
colloid. Among these, the smaller the follicles,
the darker was the autoradiographic image.
Especially, the reaction of primordial follicles
was quite strong. It is sure that the colloid in
primordial follicles is composed of newly synthesized 19s component. In fact, the new colloid represents markedly dense immunoreaction for 19s thyroglobulin. Increased size of
469
follicular lumens is reflected by increasing proportion of faster components in colloid, which
are formed by polymerization of 19s molecules
and reveal a low uptake of radioiodine, and by
decreasing accumulation of silver grains on
luminal colloid.
ACKNOWLEDGMENTS
This study was supported in part by a grant
(No. 557012) from the Ministry of Education
of Japan.
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