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Three-dimensional architecture and distribution of collagen components in the goat hypophysis.

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Three-Dimensional Architecture and
Distribution of Collagen Components
in the Goat Hypophysis
Department of Animal and Marine Bioresource Sciences, Faculty of Agriculture,
Graduate School, Kyushu University, Fukuoka-shi, Japan
Department of Plant Resources, Faculty of Agriculture, Graduate School,
Kyushu University, Fukuoka-shi, Japan
The three-dimensional architecture of collagen fibrils in the connective tissue framework
and the distribution of collagen types in the goat hypophysis were studied by the cell
maceration method in combination with scanning electron microscopy (SEM) and immunohistochemistry. The pars distalis of the adenohypophysis consisted of many cell clusters.
SEM revealed that the wall of cell clusters appeared as various-sized flat bundles of collagen
fibrils woven in a basket-like configuration. In the pars tuberalis, the aggregates of collagen
fibrils were denser and bundles thicker compared to the pars distalis. The density of collagen
fibrils changed from the pars tuberalis to pars distalis without a distinct border. The collagen
framework in the pars intermedia was mainly divided into three parts, the dorsal region with
large hollows, the middle region, and the ventral sheet facing the cavum hypophysis. In the
lobus nervosus of the neurohypophysis, the collagen network exhibited a sponge-like appearance at low magnification. Collagen fibrils of various sizes consisted of loose wavy bundles
distributed around the cavities. Immunohistochemistry revealed types I, III, IV, V, and VI
collagen throughout the hypophysis. It is concluded that to maintain structural and functional integration, the components of collagen are in different configurations throughout the
regions of the goat hypophysis. Anat Rec Part A 277A:275–286, 2004.
2004 Wiley-Liss, Inc.
Key words: collagen; hypophysis; scanning electron microscopy; immunohistochemistry; goat
Connective tissue maintains the structure and function
in a diverse range of organs and tissues. Collagen is an
important connective tissue component and interest surrounds the three-dimensional construction of the collagen
network in organs. In endocrine organs, the three-dimensional architecture of the collagen framework has been
shown in the adrenal gland (Kikuta et al., 1991) and
thyroid gland (Morita et al., 1994) using a combination of
the cell maceration method and scanning electron microscopy (SEM).
It is well known that the adenohypophysis is composed
of several types of endocrine cells and that cell aggregation forms cell cords or clusters surrounded by connective
tissue components. Although there are many studies
about adenohypophyseal cells, there are few about the
connective tissue or extracellular matrix components in
the adenohypophysis. Even those studies have mainly focused on the basement membrane components such as
type IV collagen, laminin, fibronectin, heparan-sulfate
proteoglycan, or entactin (Tougard et al., 1985; Vila-Porcile et al., 1987, 1992a, 1992b; Farnoud et al., 1992, 1994;
Horacek et al., 1993; Murray et al., 1997). Only a few
reports have described the distribution and architecture of
other members of the collagen family in the adenohypophysis (Kaidzu et al., 2000). Here, we undertook a threedimensional study of the configuration of collagen fibers in
the hypophysis.
*Correspondence to: Shotaro Nishimura, Department of Animal and Marine Bioresource Sciences, Faculty of Agriculture,
Graduate School, Kyushu University, Fukuoka-shi 812-8581, Japan. Fax: ⫹81-92-642-2942. E-mail:
Received 8 September 2003; Accepted 28 December 2003
DOI 10.1002/ar.a.20014
As in many animal species, the goat adenohypophysis is
characterized by anastomosing cell clusters and connective tissue fibers among the cell clusters (Khatra and
Nanda, 1981). The aim of this study was to elucidate the
characteristics of the three-dimensional architecture and
distribution of collagen types in the pars distalis, pars
tuberalis, pars intermedia, and lobus nervosus of the goat
hypophysis by SEM in conjunction with the cell maceration method and immunohistochemistry.
Adult Tokara goats (Japanese native breed, 7 males and
12 females) were sacrificed by exsanguinations from carotid artery under deep anesthesia with pentobarbitone.
The hypophysis was quickly removed and cut in the sagittal or frontal plane.
General Histology
For observation of the general structure, paraffin sections were prepared and classical dye staining was performed. The tissue blocks were fixed with sublimate-formalin (saturated HgCl2:formalin, 9:1) for 1 day at room
temperature and subsequently rinsed with tap water. The
tissue block was then immersed in an iodine/70% ethanol
solution for the removal of sublimate precipitate. Sections
were then dehydrated through an ethanol series and conventionally embedded in paraplast. Sections of 4 ␮m in
thickness were cut, deparaffinized with xylene, and rehydrated through an ethanol series. The trichrome staining
method described by Goldberg and Chaikoff (1952) was
employed with a slight modification.
Scanning Electron Microscopy
To observe the three-dimensional arrangement of collagen fibers, the maceration method was applied as previously described by Ohtani (1987) with a slight modification. After fixation with 3% glutaraldehyde in 0.1 M
phosphate buffer (pH 7.4) for 2– 4 days at 4°C, the tissue
was rinsed with phosphate buffer and macerated in a 7.4%
NaOH solution for 4 days at 25°C. The NaOH solution was
exchanged twice a day. The tissue was then rinsed with
distilled water for 3 days and treated with 1% tannic acid
for 2 hr followed by 1% osmium tetroxide in a cacodylate
buffer (pH 7.4) for 2 hr at 4°C. The tissue was subsequently dehydrated through an ethanol series and displaced in 2-methyl-2-propanol. Tissue was freeze-dried by
use of Tis-U-Dry Freeze-Dryer (FTS Systems). The dried
specimen was mounted on an aluminum holder and coated
with Au using an Ion Sputter IB-3 (Eiko Engineering,
Japan). Tissue sections were then observed by a Superscan SS-550 scanning electron microscope (Shimadzu, Japan) at the Center of Advanced Instrumental Analysis,
Kyushu University.
Pieces of tissue were frozen in liquid nitrogen for immunohistochemical study of the distribution of collagen
types. Tissue sections of 10 ␮m in thickness were cut by a
Leica CM1850 cryostat (Leica Instruments, Germany),
then treated with acetone (5°C, 5 min) and 1% triton
X-100 in PBS (pH 7.4) for 5 min. The ABC method was
employed for immunohistochemistry using a Vectastain
ABC kit (Vector Laboratories) in accordance with the attached protocol. Polyclonal antibovine type I, III, IV, V,
and VI collagen antisera (LSL, Japan) were used at a
working dilution of 1:1,000. The specificity of the immunostaining was confirmed by omission of the primary antiserum.
Pars Distalis of Adenohypophysis
The pars distalis of adenohypophysis was composed of
many cell clusters. The clusters packed several to dozens
of glandular cells and were irregular in shape and of
varying size (Fig. 1A). Cell clusters were enclosed with
connective tissue components stained with aniline blue
using trichrome staining. Sinusoids distributed in the interspace of cell clusters did not penetrate into the clusters.
The zona tuberalis, which was distinguished from other
regions of the pars distalis by the predominant basophils,
was observed in the rostroventral region of the gland (data
not shown). No gender difference in the connective tissue
profile was apparent in this preparation.
NaOH maceration retained no cell components for SEM.
The collagen framework was seen throughout the gland.
At low magnification, a cell cluster was evident as a basket-like compartment (Fig. 1B). The residual space of
glandular cells in a cell cluster was continuous and their
border was not always obvious because of the lack or
complete absence of collagen septa in the cell cluster (Fig.
1C). At a high magnification, dozens of collagen fibrils
could be observed as made up out of various-sized flat
belt-like bundles. The bundles intersected each other randomly (Fig. 1D). A fine and irregular collagen fibril net
covered the inner surface of the basket.
In the pars distalis, a thick layer of connective tissue lay
between large blood vessels and cell clusters (Fig. 2A,
arrowheads). The wall of the large blood vessel was reinforced with a tough and continuous sheet of collagen with
a rugged inner surface (Fig. 2B). In this collagen sheet, a
thin net-like configuration of fibrils in the innermost layer
covered the underlying layer of thicker bundles in a predominantly circular direction (Fig. 2C and D). The rugged
surface was attributed to variation in bundle thickness,
being dense and tough in some places and loose and thin
in others (Fig. 2D). In comparison, sinusoids lay among
cell clusters and shared the collagen wall with neighboring cell clusters (Fig. 2E). Fine solitary fibrils were entwined on the inner surface of the wall like the large
vessel, although the density was relatively less than in the
latter (Fig. 2F).
The ventral capsule of the gland, part of the dura mater,
consisted of a stack of many collagen sheets in parallel to
the gland surface (Fig. 3A). In each sheet, components of
the sheet were formed from collagen fibrils in a predominantly transverse arrangement and dense aggregation of
collagen bundles (Fig. 3B).
Light microscopy showed that the marginal layer facing
the cavum hypophysis was lined with a single cuboidal or
columnar layer of epithelium on a connective tissue layer
(Fig. 4A). Under low-magnification SEM, the underlying
collagen sheet was seen as a flat plate of densely packed
collagen fibrils (Fig. 4B and C). In the collagen plate, the
delicate surface appeared as a cloth of collagen fibrils and
thin bundles (Fig. 4D and E). A tough supporting layer
was composed of thick collagen bundles crossing over each
other (Fig. 4B).
Fig. 1. Light and scanning electron micrographs of the pars distalis in
the goat adenohypophysis. A: Light micrograph of pars distalis using
trichrome staining. Sinusoids (arrowheads) are distributed among cell
clusters (asterisks) in the surrounding connective tissue. Scale bar ⫽ 50
␮m. B: Scanning electron micrographs of the pars distalis. The wall of
cell cluster is seen as aggregations of basket-like collagen fibrillar bun-
dles. Scale bar ⫽ 50 ␮m. C: High magnification of the white frame in B.
Collagen fibrils are mainly composed of the wall of each cell cluster
(asterisk) and there are few inside. Scale bar ⫽ 10 ␮m. D: Larger
magnification of the white frame in C. Single or a few collagen fibrils are
randomly seen on the surface of the belt-like bundles. Scale bar ⫽ 2 ␮m.
Fig. 2. Light and scanning electron micrographs of a blood vessel
(BV) in the pars distalis. A: Light micrograph of a large blood vessel and
surrounding parenchymal tissue using trichrome staining. Connective
tissue layer (arrowheads) intervenes between BV and cell clusters (asterisks). Scale bar ⫽ 50 ␮m. B: Scanning electron micrograph of the
blood vessel and surrounding collagen framework. Scale bar ⫽ 20 ␮m.
C: High magnification of the surface of the BV in B. Collagen bundles
were wavy and circularly coursed along the longitudinal axis. Scale
bar ⫽ 5 ␮m. D: High magnification of the surface of large blood vessel.
Collagen fibrils are randomly entwined like a net in the bundle surface.
Scale bar ⫽ 2 ␮m. E: The vestige of sinusoids (arrowheads) among cell
clusters. The sinusoid is usually adjacent to cell clusters. Scale bar ⫽ 50
␮m. F: High magnification of the white frame in E. Scale bar ⫽ 5 ␮m.
Fig. 3. Ventral capsule (VC) of the pars distalis (PD). A: Sagittal section of the VC shows it is composed
of many layers of collagen sheets. Scale bar ⫽ 100 ␮m. B: High magnification of the white frame in A. Most
of the fibrils are arranged circularly along the longitudinal axis of the gland. Scale bar ⫽ 20 ␮m.
Pars Tuberalis of Adenohypophysis
The pars tuberalis is situated in the cranial region of
adenohypophysis close to the median eminence. Histological sections showed that cell clusters were relatively
small compared to those of the pars distalis (Fig. 5B). SEM
showed that the smaller hollow with no glandular cells in
the pars tuberalis was surrounded by a thicker wall of
densely packed collagen bundles compared with the pars
distalis (Fig. 5A). These features were also observed in the
interclusteral band of connective tissue stained with aniline blue (Fig. 5B). This thicker wall of collagen bundles
was predominant in the proximal region, where varioussized bundles intermingled with a random strand (Fig. 5C
and D). However, a distinct border with a special configuration of collagen bundles could not be determined between the pars tuberalis and pars distalis.
Pars Intermedia of Adenohypophysis
In histological specimens, the pars intermedia was in
contact with the dorsal neurohypophysis through an intervening connective tissue layer, with branches penetrating the pars intermedia as septa carrying blood vessels
(Fig. 6A). SEM showed the collagen framework of the pars
intermedia had a rough dorsal region with large hollows,
a middle region with many branches, and a ventral sheet
facing the cavum hypophysis (Fig. 6B). In the dorsal region, flat collagen sheets separated the gland into many
compartments or lobules with few branches of collagen
fibrils or bundles. In the middle region, many branches of
fibrils and bundles from the collagen sheets made up a
loose collagen mesh (Fig. 6C). The collagen sheet was
composed of intermingled collagen fibrils and bundles and
some circular strands (Fig. 6D and E). The ventral collagen sheet in the pars intermedia over the cavum hypophysis had many pores in contrast to the opposite sheet of
the pars distalis (Fig. 6B, arrowheads).
Lobus Nervosus of Neurohypophysis
The neurohypophysis was placed on the dorsal side of
the adenohypophysis as described for the pars intermedia.
Histological section in the sagittal plane showed that the
connective tissue of the lobus nervosus was wavy and ran
along the nerve fibers and encircled nerve fibers in the
frontal section (Fig. 7A and B). Blood vessels were usually
accompanied by thick connective tissues. Low-magnification SEM showed the collagen network in the lobus nervosus had a sponge-like appearance with felt-like collagen
platelets and bundles enclosing various-sized cavities
(Fig. 7C). The felt-like platelets of the collagen fibrils were
observed in many places and thin collagen bundles rose to
distribute around cavities (Fig. 7D). Wavy or spiral collagen bundles were very common. Fibrils and bundles of
various sizes intermingled with each other to form a loose
network (Fig. 7E). The course of capillary vessels were not
obvious in the SEM specimen.
Fig. 4. Light and scanning electron micrographs of the marginal layer
of PD facing the cavum hypophysis (CH). A: Sagittal section of PD and
pars intermedia (PI). The marginal layer of PD is composed of a single
cuboidal or columnar epithelium and lining connective tissue layer. Scale
bar ⫽ 50 ␮m. B: Scanning electron micrographs of the connective tissue
layer lining the marginal layer. High magnification of the white frame in C.
The connective tissue layer is composed of a few layers of thick bundles
of collagen fibrils. Scale bar ⫽ 4 ␮m. C: Low magnification of the surface
of the marginal collagen layer. Scale bar ⫽ 50 ␮m. D and E: High
magnifications of the surface of the layer. Scale bars ⫽ 100 ␮m and 2
␮m, respectively.
brane. Immunolabeling by other antisera was detected in
the remaining regions of connective tissue in the hypophysis. The distribution of all collagen types except for type
IV was very similar and we could not distinguish specific
Type I, III, IV, V, and VI collagen antisera labeled the
connective tissue compartments of all regions of the adenohypophysis and neurohypophysis (Fig. 8). Here, only
type IV collagen antiserum labeled the basement mem-
Fig. 5. Light and scanning electron micrographs of the pars tuberalis
(PT) in the goat adenohypophysis. A: Scanning electron micrograph of
PT in the sagittal plane. In the PT, the aggregation of collagen fibrils is
denser and thicker than in PD. Scale bar ⫽ 100 ␮m. B: Light micrograph
of the sagittal section of PT with trichrome staining. Cell clusters in this
region are relatively smaller in size and there are more connective tissue
components compared to the PD (see Fig. 1A). Scale bar ⫽ 50 ␮m. C:
High magnification of a part of the PT in A shows dense aggregations of
collagen fibrils. Scale bar ⫽ 40 ␮m. D: High magnification of the white
frame in C. Scale bar ⫽ 4 ␮m.
three-dimensional organization of the reticular fibers in
the human pancreas (Ohtani, 1987). Although collagen
frameworks in many tissues have been studied using this
The maceration method with NaOH solution was first
developed for use in conjunction with SEM to image the
Fig. 6. Light and scanning electron micrographs of PI in the goat
adenohypophysis. A: Light micrograph in the sagittal section shows the
PI is separated from the lobus nervosus (LN) by an intervening connective tissue layer (arrowheads) on the dorsal side. B: Scanning electron
micrograph of the PI in the sagittal plane. Many holes were observed in
the ventral sheet (arrowheads). Scale bar ⫽ 500 ␮m. C: High magnifi-
cation of the white frame in B. Elongated flat collagen sheets (arrows)
project downward from the dorsal sheet and thinner bundles (arrowheads) and irregularly branch from the frames. Scale bar ⫽ 50 ␮m. D and
E: Higher magnifications of a collagen sheet in the PI. The frames are
composed of irregularly coursed collagen fibrils. Scale bar ⫽ 4 ␮m and
2 ␮m, respectively.
Fig. 7. Light and scanning electron micrographs of the lobus nervosus in the goat neurohypophysis. A and B: Light micrographs in the
sagittal (A) and frontal (B) plane. Sagittal section shows that the connective tissue is wavy (arrowheads in A) and surrounds some nerve fibers in
the frontal section (arrowheads in B). Scale bar ⫽ 50 ␮m. C: Low-
magnification scanning electron micrograph of the lobus nervosus.
Scale bar ⫽ 100 ␮m. D: High magnification of the lobus nervosus in C.
Scale bar ⫽ 20 ␮m. E: High magnification of the white frame in D. Scale
bar ⫽ 4 ␮m.
Fig. 8. Light micrographs of the goat hypophysis immunolabeled with anticollagen types I (A–C), III (D–F),
IV (G–I), V (J–L), and VI (M–O). A, D, G, J, and M show labeling in the pars distalis. B, E, H, K, and N show
labeling in the pars intermedia. C, F, I, L, and O show labeling in the lobus nervosus. Scale bar ⫽ 30 ␮m.
method, the three-dimensional architecture of collagen
has only been reported in the endocrine organs of the
adrenal gland (Kikuta et al., 1991) and thyroid gland
(Morita et al., 1994). Here, we present the first data on the
three-dimensional architecture of collagen fibers in the
The pars distalis is the aggregation of cell clusters composed of glandular cells enclosed by connective tissue.
Some organs, such as the adrenal gland and liver, also
have cell clusters as their components. Although the adrenal gland has cell clusters in the zona glomerulosa, zona
fasciculata, and zona reticularis of the adrenal cortex and
adrenal medulla, the architecture of the collagen framework around cell clusters changes according to cord structure (Kikuta et al., 1991). The collagen architecture of the
pars distalis shown in the present study is similar to that
of adrenal medulla. In the liver, the architecture of the
wall of space occupied by hepatocytes (Ohtani, 1988) is
similar to that in the pars distalis seen here, although the
residual space of hepatocytes is not basket-like but tubelike. In comparison, the thyroid gland has follicles lined
with a simple cuboidal epithelium. The follicles are surrounded by perifollicular collagen sheaths composed of
both thick collagen bands that run in various directions
and fine solitary collagen fibrils (Morita et al., 1994). It
also has an architecture similar to that found in the pars
distalis. From these results, the basket-like architecture
of the collagen framework is common in holding glandular
cells in various endocrine organs.
Sinusoids are generally distributed according to the endocrine function of the gland. SEM revealed that the hepatic sinusoid is surrounded with a wall of intermingled
collagen and the collagen meshwork lining the hepatic
sinusoids is characterized with many switchback fibrils in
human and rat liver (Ohtani, 1988). On the other hand,
such switchback pattern of fibrils were not so predominant in the collagen meshwork for adenohypophyseal
blood vessels or sinusoids in this study. As hepatic sinusoids also have structural relationship with the spaces of
Disse (Ohtani, 1988) but there are no such spaces in the
adenohypophysis, the difference in the collagen meshwork
for sinusoids may reflect the structure and function of
liver and adenohypophysis. In the pars distalis, the density of solitary fibrils surrounding the inner surface of
vessels seemed to change according to the size, namely,
they are denser in the large vessel and are sparser in the
small vessels or sinusoids (Fig. 2D and F). It may be
related to the structural strength of vessels.
The pars tuberalis occupies the cranial region of the
gland, to some extent enclose the infundibulum, and has
an important role in connecting the pars distalis to the
hypothalamus. It also strengthens the tissue by increasing collagen levels. In this study, SEM revealed the reinforcement of the pars tuberalis with many collagen fibrils
and that this tough architecture may have a greater effect
on the smaller cell clusters compared to those in the pars
The collagen sheets surrounding the large parenchyma in the pars intermedia had a unusual structure
and were different from any other in hypophyseal regions. Although the compartment in the dorsal region
contained either no or only a few collagen branches, the
parenchyma in the middle region appeared to be supported by a coarse network of collagen branches. As the
cavum hypophysis intervenes between the pars intermedia and pars distalis and the ventral surface of pars
intermedia is free from pars distalis except for the lateral periphery in the goat hypophysis (Khatra and
Nanda, 1981), many more collagen branches strengthen
the structure of the middle region in the pars intermedia compared to the dorsal region.
Interestingly, the architecture of the surface sheet of
collagen in the side of the cavum hypophysis was different
in the pars distalis and pars intermedia. The surface in
the former was uniformly flat while the latter had scattered pores. As there is a layer of epithelium on this
surface in the intact organ, it indicates that epithelial cells
in some regions on the side of the pars intermedia are
directly attached to glandular cells in the pars intermedia.
The significance of this structure remains to be determined.
The neurohypophysis is composed of neural tissue extending from the hypothalamus. As far as we know, there
are no reports describing the three-dimensional architecture of collagen in the central nervous system. The present
study showed that the architecture of the collagen network in the lobus nervosus of the neurohypophysis had a
sponge-like configuration and that collagen bundles had a
wavy or spiral profile. This architecture appears to be
more flexible compared to that found in the cell cluster of
the pars distalis and may determine the function of neural
Although positive immunolabeling was detected
throughout the goat hypophysis with type I, III, IV, V, and
VI collagen antisera, we could not identify the type of
individual collagen fibrils in the macerated specimen either morphologically or immunohistochemically. As the
maceration method removes all of the cellular elements,
including their basal lamina (Ohtani, 1988), the type IV
collagen component of the basal lamina may not reside in
the macerated specimen. Thus, the macerated hypophyseal specimen consisted of at least four other types of
collagens. An appropriate method is needed to clarify the
distribution of each collagen type in the macerated specimen.
Despite reports that show tumor GH3B6 prolactin cells
produce basement membrane components in vitro (de Carvalho et al., 2000) and primary cultured adenohypophyseal cells in rat synthesize types I and III collagens
(Kaidzu et al., 2000), the synthesis and secretion of collagen components by adenohypophyseal cells have not been
demonstrated in vivo. The present study showed an absence of immunolabeling for any type of collagen in the
adenohypophyseal cells. Kaidzu et al. (2000) suggested
that collagen turnover in the adenohypophysis was slow in
vivo and that the cells might monitor their environment
and levels of collagen. During synthesis, collagen is modified from a large-molecular-weight precursor into procollagen, which has additional nonhelical polypeptide domains, before and after secretion (Davidson and Berg,
1981). Therefore, it may be available to detect the procollagen molecule or its mRNA for the identification of collagen-producing cells. More research will be needed to clarify this.
In conclusion, we have shown that the architecture of
the collagen framework varies between the adenohypophyseal pars distalis, pars tuberalis, and pars intermedia and neurohypophyseal lobus nervosus of the
goat. This variation throughout the hypophysis may
reflect a difference in their functions or topographical
properties. Further investigation will determine differences in the development of collagen architecture in the
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architecture, hypophysial, dimensions, distributions, components, three, goat, collagen
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