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Histochemical and Ultrastructural Observations of Respiratory Epithelium and Gland in Yak (Bos grunniens).

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THE ANATOMICAL RECORD 293:1259–1269 (2010)
Histochemical and Ultrastructural
Observations of Respiratory Epithelium
and Gland in Yak (Bos grunniens)
Faculty of Veterinary Medicine, Gansu Agricultural University, Lanzhou, Gansu, China
Submucous glands and epithelial mucous cells of yak (Bos grunniens)
respiratory tract have been studied by a variety of histochemical methods
and transmission electron microscopy for differentiating and characterizing serous and mucous cells. By light microscopy, the distribution, numbers of mucous cells, volume of mucous glands (Reid index), and the ratio
of mucous cell to serous cell in the bronchial tree were measured with different staining. Histochemically, a majority of mucous cells, presented in
the surface epithelium of bronchi and glands, secreted neutral and acid
mucosubstances, only a few sulfated mucosubstances were present. No
mucus-producing cells were observed from the terminal to respiratory
bronchiolar level. Ultrastructurally, serous cells in glands of the lamina
propria had two distinct forms: one type filled with many round dense secretory granules, plentiful RER and few other organelles, similar to other
animals; the other type contained some oval mitochondrial and distended
RER, the granules resembled the former. The mucous cells in gland were
similar to that of epithelium, which containing abundant secretory granules with an eccentric core. The mucous cells of the surface epithelium
differ from other animals in the structure and histochemistry of their secretory granules. Analysis of the size and distribution of the secretory
granules and other organelles of serous cells suggested that differences
represent different phases of a secretory cycle, not various populations of
C 2010 Wiley-Liss, Inc.
cell or granules. Anat Rec, 293:1259–1269, 2010. V
Key words: respiratory
ultrastructure; yak
The surface of bronchial tree is coated with a layer of
respiratory tract mucus containing electrolytes, proteins,
and glycoproteins. The mucus is thought to be provided
a mechanical barrier between airborne particles or gaseous products and the cilia, as well as the apical cell
membrane for protecting the airways against inhaled irritant gases and particles, and changes in the temperature or humidity of inspired air.
Comparative studies have shown that the abundance,
distribution, and contents of secretory cells vary considerably among different kinds of species. It has been
studied in several mammals, rodents (Dalen, 1983;
McCarthy, 1964; Plopper et al., 1984), carnivores (Gatlagher et al., 1975; Robinson et al., 1986), primates
(George et al., 1986; Plopper et al., 1989), domestic animals (Jones et al., 1975; Mariassay et al., 1988; Kahwa
and Purton, 1996; Raji and Naserpour, 2007) and man
(Lamb and Reid, 1972).
Grant sponsor: The National Natural Science Foundation of
China; Grant number: 30571342; Grant sponsor: Natural
Science Foundation of Gansu Province; Grant number: 0802-02.
*Correspondence to: Yan Cui, Faculty of Veterinary Medicine,
Gansu Agricultural University, Lanzhou 730070, Gansu, China.
Fax: 86 931 7631220. E-mail:
Received 27 May 2009; Accepted 27 September 2009
DOI 10.1002/ar.21056
Published online 28 April 2010 in Wiley InterScience (www.
Fig. 1. Bronchial wall of five-month-old yak stained with H.E. The mucous cells (Arrows) were stained
blue. BV, blood vessels; Ca, cartilage; E, epithelium; G, glands; SM, smooth muscle.
The yak originated in the Qinghai-Tibetan plateau of
the People’s Republic of China. Approximately 14 million
yaks are found in China, accounting for 90% of the total
number of yaks in the world. Yaks play an important
role in both livelihoods and natural ecosystems of the
Qinghai-Tibetan plateau. But there is no related information available on Yak. The purpose of this study was
to characterize the histochemical composition and the
ultrastructure of bronchial surface epithelium and submucosal glands of the yak in order to make basic information for comparison with other mammalians.
Five clinically normal, age between 5 and 6 months
yaks of both sexes, from local farmer in Datong County
of Qinghai Province, were used in this study. All animals
were killed by exsanguinations via the abdominal aorta
in slaughter house. The lungs were obtained immediately after the subjects were killed and fixed by tracheal
infusion of 4% neutral paraformaldehyde phosphate
buffer (pH 7.3) at 30 cm water pressure for 2 hours,
then stored in the same fixative for one month.
For light microscopy, the samples were taken randomly from the caudal lobe of the left lung, and then cut
into pieces no larger than 1 cm3. Representive portions
of each lung were dehydrated in graded alcohol and embedded in paraffin wax, serially sectioned at 4 lm. Every
sixth section was mounted and stained with Alician blue
(AB pH 2.5, 30 min) and periodic acid Schiff reaction
(PAS). At intervals along the airway additional sections
were also stained with either standard haematoxylin
and eosin (HE) to examine the general morphology
(Figs. 2A and 3A), or with AB at pH 1.0 to characterize
further the histochemical nature of the epithelial cells,
or even with Toluidine blue to examine the metachromasia of mucosubstances.
The mucous cell density of airway epithelium was estimated by counting mucous cell nuclear profiles in 100
lm of basal lamina lining each airway (Mariassay and
Plopper, 1983), and in submucosal glands the mucous
and serous cell were also counted. The measurement of
the gland to wall ratio was described by Reid (1960),
which is generally referred to as the Reid index. The
Reid index is expressed as ratio of the thickness of
the gland to the distance between the basement and the
inner aspect of cartilage (Reid, 1960; Shimura, 1990).
Fig. 2. Bronchial glands of five-month-old yak with H.E A: PAS/AB pH2.5 B: PAS C: AB pH2.5 D: AB
pH1.0 E: and Toluidine blue F: staining. Ca, cartilage; M, mucous cells; S, serous cells.
The epithelium was photographed and the length of the
basal lamina of the counted regions was determined
with Olympus DP71 microscopy (including DP control
and Image-Pro Express), and expressed with mean SD.
For transmission electron microscopy, tissue samples
were taken randomly from the caudal lobe of the left
lung immediately after slaughter, cut into pieces of
approximately 1 mm3 immersed in 2.5% glutaraldehyde
in neutral phosphate buffer (pH 7.3, at 4 C) and
Fig. 3. Mucous cells of bronchial epithelium of five-month-old yak stained with H.E A: PAS/AB pH2.5
B: PAS C: AB pH2.5 D: AB pH1.0 E: and Toluidine blue F: C, ciliated cells; M, mucous cells.
postfixed in 1% osmium tetroxide for 2 hours. The tissue
was dehydrated in graded ethanol and embedded in
Epon812. Orientation of the block was achieved by
examining 1 lm sections stained with Toluidine blue.
Thin sections (60–80 nm) were cut on a Leica EM-UC6
ultramicrotome, mounted on G200 grids, stained with
alcoholic uranyl acetate and lead citrate and viewed
with a JEOL 1230 electron microscope at 120 kV.
TABLE 1. Histochemical reaction of submucous glands and epithelium mucous cells
McManus, 1948
pH 2.5
Mowry, 1956
a few stained Red
AB pH 2.5
Lev and Spicer,
Lev and Spicer,
Many cells red or
a few stained blue
Mostly unstained,
some blue
More cells unstained
compared to AB pH
2.5, a few blue
Mostly unstained, some
purple (metachromasia)
AB pH 1.0
Tock and Tan,
Interpretation of
staining reactions
Mucous cells
Most cells light blue,
a few unstained
Purple (metachromasia)
Periodate-reactive carbohydrates
and/or glycogen
To seperate acidic glycoconjugates
(carboxylated and/or sulphated
glycoconjugates) from neutral types
Acidic glycoconjugates (carboxylated
and sulphated types)
Sulphated acidic glycoconjugates
Sulphated acidic glycoconjugates
TABLE 2. Number of mucous cell profiles in bronchial airways of yak
Small Bronchi
Gland (%)
AB pH 2.5
AB pH 1.0
7.3 2.3a
4.8 1.4
17.4 6.5b
6.9 2.2
4.4 2.2
16.5 7.5
7.3 1.8
4.1 2.0
17.4 6.9
Number of mucous cell profiles in bronchial epithelium of yak in per 100 lm.
Proportion of mucous cell profiles in submucous glands in lung of yak.
The results of the histochemical reactions and number
of mucous cells in bronchial airways obtained are summarized in Table 1.
Submucosal Glands
Light microscopy. The yak airways had extensive
submucosal glands which lay between the muscle and
the epithelium and/or the muscle and the cartilage, little
or no penetration of the glands into the muscle layers
(Fig. 1). The gland to wall ratio (Reid index) was 23.6 8.3 percent. These tubulo-alveolar glands, composed of
two types of secretory cells, serous and mucous, were
present throughout the tracheobronchial tree except in
the terminal airway and respiratory bronchioles. They
were numerous in the larger bronchi. The ratio of mucous to serous cells in gland acini with various staining
is in Table 2. They were all stained red with PAS (Fig.
2C), with some whole acini or cells within an acinus
staining with AB pH 2.5 as well (Fig. 2D). The majority
of the cells in these glands were stained red or reddishpurple in the PAS-AB reaction. The staining was restricted to the apically localized granules, showing the
presence of neutral mucin in them (Fig. 2B). There were
however a smaller number of glandular cells in the
bronchus, which contained acidic mucus. The AB pH 1.0
staining showed that few of cells contained sulphated
mucin in submucosal glands (Fig. 2E).
Electron microscopy. Two distinct granule types
could be seen, electron-dense granules in serous cells
and electron-dense granules with an eccentric core in
mucous cells. The mean size of the serous granules for
each cell was usually smaller than that of mucous granules. A cross section of a single acinus could contain
either mucous or serous cells, or a mixture of cell types
adjacent to each other (Fig. 4).
Serous cell. In cross-sections, the serous cells were
arranged around a small central lumen (Fig. 7). On the
basis of differences in their cytoplasmic inclusions, two
distinct forms of serous cells were recognized.
The common serous cell (Fig. 5) had a round or elliptical nucleus, basal in position and with a prominent
nucleolus. The serous cells contained numerous secretory granules, usually concentrated toward the apex of
the cell. Although they were densely packed they did
not distend the cell as in mucous cells. Individual granules were usually round and completely surrounded by
a membrane. Granules were seen close to the unit
membrane of the apical cell surface, whereas the mucous cell granules were often seen open and discharging. The mitochondria were round and ovoid; they were
mainly concentrated in the base of the cell, but a few
were found among the granules. Most of the rough
endoplasmic reticulum (RER) was at the cell base, the
cisternae being narrow and grouped in parallel arrays
(Fig. 5). Free ribosomes were abundant through the
cytoplasm. The Golgi apparatus was well developed and
supranuclear, often with dilated lamellae and many
associated vesicles. Multivesicular bodies were seen
The second type of serous cell was uncommon (Fig. 8),
the nucleus was indented in shape, also basal in position
and with a prominent nucleolus, but the cytoplasm was
slightly dense than that of common one. The apical portion of the cell packed with abundant secretory granules,
and many round mitochondria were observed among
them. Plenty of dilated RER filled with the basal area.
Golgi apparatus and multivesicular bodies were rarely
The cells of the epithelium were linked at their luminal surface by tight junctions, and throughout the depth
Fig. 4. Yak bronchial gland with two types of cells A: mucous cell
(M) and serous cell (S). The nuclear (N) of mucous cell was compressed at basal side B:. Numerous secretory granules (SG) located
at the apical portion of cells, the sizes of dense granules of mucous
cell with lucent core bigger than that of serous cell (B). The serous
cells contained rough endoplasmic reticulum (RER) at basal portion
and vacuoles (V) in perinuclear area b, C:. Smooth endoplasmic reticulum (SER), RER and mitochondrial (M) present among the granules of
mucous cell D. GC, glandular cavity
of the epithelium there was a degree of interdigitation
between adjacent cells, with desmosomes occasionally
being seen in Figure 6.
lescing secretory granules (Fig. 4D). These granules
contained an electron-dense granular matrix that surrounded a finely granular, with a round and eccentric
electron-lucent core. In addition to granules, the cytoplasm contained mitochondria, small amounts of RER;
occasionally a Golgi apparatus would be noted in
the cytoplasm. The cytochemical reactivity of the granules was similar to the mucous cells of the epithelial
Mucous cell. The mucous cell had a columnar shape
(Fig.4B), resembled that of the epithelial surface. Its
nucleus was compressed at the basal side and was
irregular in outline, with dense chromatin. The cytoplasm of the columnar cell was filled with large un-coa-
Fig. 5. Well-developed RER located at the basal portion of serous
cell. BM, basement membrane; N, nuclear; SG, secretory granules; V,
Fig. 6. Juction complex (JC) of serous cell and adjacent cells, intermediate junctions and desmosomes were present.
Fig. 7. Another type of serous cell (Stars) in bronchial gland with
plentiful distended RER and apical secretory granules.
Fig. 8. Two types serous cell in bronchial gland. Numerous secretory granules (SG) and abundant mitochondrial present at supranuclear and distended RER (Triangle) surrounded the dentated nuclear
(N) in serous cell (Top). The common serous cell with abundant RER,
some mitochondria (M) and secretory granules (SG).
Epithelial Mucous Cells
Light microscopy. There were a large number of
mucous cells of the surface epithelium in the bronchi
and the bronchioles (Table 2), whereas no mucous cell
was observed in terminal and respiratory bronchioles.
Mucous cells were characterized by the presence of
Alcian blue and/or PAS-positive granules. The majority
of mucus-containing cells in the bronchi and bronchioles
were stained blue with AB pH 2.5 showed that containing acidic mucosubstances (Fig. 3D), or red with the PAS
showing the neutral mucosubstances in them (Fig. 3C).
Fig. 9. Mucous cell in bronchial epithelium of yak contained basal nuclear and abundant dense secretory granules (SG) with a lucent core (A). Mitochondrial (M) and RER were also observed (B). C, ciliated
cell; Ci, cilia; GL, globular leukocyte; N, nuclear.
PAS decreased distally along the airways. Although no
cells staining only with Alcian blue were seen, an alcianophilic layer was present at the epithelial-luminal
interface at all levels of the airways, and appeared to lie
over all types of cell.
Electron Microscopy
Serous sell. No serous cells were observed throughout the whole airways epithelium.
Fig. 10. Mucous cell in bronchial epithelium had numerous
vacuoles (V) among secretory granules (SG). C, ciliated cell; Ci, cilia;
N, nuclear.
In the combined AB-PAS staining these cells stain blue
or bluish-purple (Fig. 3B). However, the AB pH 1.0
showed that the majority of the goblet cells had sulphated mucin. These cells stained blue or light blue (Fig.
3E). Cells staining only with Alcian blue were never
seen, whilst the proportion of cells staining only with
Mucous cell. Mucous cells were columnar cells with
a microvillar surface, abundant cytoplasm, and a basal
nucleus. The nucleus, looked oval in shape and contained electron-dense chromatin, was located immediately
above the basal cell layer and below the level of the ciliated cell nuclei (Fig. 9). The cytoplasm was composed
mostly of secretory granules. Mitochondria and RER were
dispersed throughout the cytoplasm. Golgi apparatus
were occasionally present. Mucous granules were roughly
round membrane-bound structures. Some granules contained an eccentric lucent core (Fig. 9B). Some, less-frequent, mucous cells cytoplasm contained perinuclei Golgi
apparatus, mitochondria, numerous specific vacuoles,
amounts of distended RER, and few number of membrane-bound dense granules (Figs. 10 and 11).
Submucosal Glands
Through extensive examination of tissue sections
detected from lung of yak, we found there were substantial numbers of submucosal glands along tracheobronchial trees in this species of animals. Similar
observations as previously reported in camel (Raji and
Naserpour, 2007), sheep (Mariassay and Plopper, 1984),
Serous Cell
Fig. 11. Mucous cell in bronchial epithelium had a basal dentate
nuclear (N) with distended RER surrounded and many secretory granules (SG) at apical area. C, ciliated cell.
goat (Kahwa and Purton, 1996), cat (Gatlagher et al.,
1975), dog (Takenaka et al., 1996) and ferret (Robinson
et al., 1986). There are variables between different species of animals. Submucosal glands in the treachea of
the horse are known to be smaller than that of other
mammalian species (Widdicombe and Pecson, 2002), and
no similar gland had been reported in buffalo lung
(Singh and Mariappa, 1981). In case of mice, some
glands only had been discovered at the border between
the trachea and the larynx (Choi et al., 2000), agreement
with the findings of Pack et al (1980). For rat, the glands
were present in the cranial third of the trachea, and the
number of glandular tissues may increase near the carina (Steiger et al., 1995; Ohtsuka et al., 1997; Choi
et al., 2000). In respect to guinea pig, there were some
contradictions: some have reported that the glands of
guinea pig were present in the trachea (Okamura et al.,
1996; Widdicombe et al., 2001). Others believed that the
tracheal submucosal glands in guinea pig were infrequent or even absent (Jeffery, 1983; Yeadon et al., 1995).
Kennedy et al. (1978) claimed that they noted the distribution of glands in the hamster, which can be found in
the trachea and the larynx, but very rare in the rest of
the tracheobronchial tree. For small animals, such as
rabbits, hamsters, rats and mice (Borthwick et al., 1999;
Widdicombe et al., 2001) findings of submucosal gland
were infrequent, and if they did appear, their appearances only occurred in the uppermost portion of the trachea. A significant correlation has been found between
airway diameter and gland volume per unit surface area
of trachea in different of species, such as ox, goat, sheep,
pig, monkey, dog, cat, rabbit, guinea pig, hamster, rat,
mouse, and human, suggesting that the rate of deposition of inhaled particles may increase in large airways
(Choi et al., 2000; Widdicombe et al., 2001).
As aforementioned, under electron microscopic observations, two different types of serous cells in submucosal
glands of yak lung are discernible. First type is termed
as common serous cells, and second type as uncommon.
Serous cells in yak lung were found only in submucosal
glands resembled sheep (Mariassay and Plopper 1984).
These cells filled with densely packaged granules,
whereas in sheep it contained electron-dense granules
with a more electron-dense core. In mice, submucosal
gland usually contained only one form of secretory granulewhich produced either mucous or serous substance. It
was confirmed that the number of secretory granules
varied possibly reflecting different states of synthesis or
discharge, whereas a cell was almost devoid of granules,
the cytoplasm was filled with a dense array of SER. In
man bronchus tree, the volume of serous and mucous
cells in glands was about 61 to 39% (Basbaum et al.,
1990). As reported by some investigators, serous cells
had electron-dense cytoplasm, more RER, in contrast
with that of mucous cells, granules of which were
described as discretely electron-dense and measured
300–1000 nm in diameter (Rogers et al., 1993; Jeffery
and Li, 1997; Finkbeiner, 1999). Serous and mucous cells
in the lung of yaks were calculated to be approximately
83% and 17% in the volume of the glands (Table 2). In
addition, the second type serous resembled that of ferret
(Basbaum, 1986), the common serous cells were similar
to other animals.
Mucous Cells
At the TEM level, most mucus-producing cells contained a mixture of both serous (electron-dense) and mucous (electron-lucent) secretory vesicles. In the yaks,
mucous cells, which are present in surface epithelia and
submucosal glands, were found to include secretory
granules. They appeared to be electron dense with
lucent core and uncoalescing. The findings were agreement with the observation of the previous study (He
et al., 2009). However, what is seen in the lung of yaks
differs from granules in other species reported by others,
such as sheep (Mariassay et al., 1988), monkeys (Wilson
et al., 1984; Plopper et al., 1989), and rodents (Kennedy
et al., 1978; Dalen, 1983). Mucous cells in sheep were
classified into four types. Granules in mucous cells of
types M1 and M2 had a less electron-dense meshwork,
whereas granules in types M3 and M4 were electronlucent with electron dense cores. For Bonnet monkey,
mucous granules were membrane-bound structures containing a centrally dense core, with occasional coalescing. In Rhesus monkey, mucous cells were filled with
membrane-bound granules of variable electron densities.
They were either biphasic or triphasic granule with a
lucent rim and cores. Granules in guinea-pig and hamster mucous cells were all membrane-bound with a characteristic electron-dense cores, the former coalesced near
the cell surface, but the latter did not coalesce. In mouse
and rat, the goblet cells were rarely found in treacheobronchial tree, electron lucent incomplete membranebound secretory granules with an electron-dense core
were often confluent. Electron-dense cytoplasm containing confluent granules of electron-lucent with about
800 nm in diameter were reported in mucous cells of
man by Jeffery and Li (1997). The electron density and
a series of different staining (PAS) of granules mucous
cells in the glands and surface epithelium suggest that
the cells are probable of the same phenotype. In the
report by Staley and Trier (1965) who used AB/PAS
staining a similar correlation between PAS reactivity
and electron density for part of the ‘two-toned’ granule
of the mouse Paneth cell, showed that the outer electron-lucent halo of the granule contained an acid mucosubstance (AB-positive), whereas the inner electrondense core contained a neutral protein (PAS-positive).
Mucus Property
The histochemical results shown here reveal three
types of mucosubstances in yak tracheobronchial tree.
These were neutral mucins, acidic mucins, and sulphated mucins.
The nature of the mucosubstances of submucosal
glands seen in this study was similar to those of many
other species reported already. In yak, the mucosubstances of mucous cells in submucosal gland were strongly
positive with PAS and/or AB and toluidine blue staining,
whereas the serous cells were positive with PAS and
negative with AB and toluidine blue staining. In goat,
submucosal glands produced predominantly acidic mucosubstances with only a few producing a mixed reaction,
neutral mucosubstances were rarely observed (Kahwa
and Purton, 1996). Serous cells were found exclusively
in submucosal glands in sheep, which stained light magenta with AB/PAS. The staining was restricted to the
apically localized granules (Mariassay et al., 1988). In
dog, a mixture of sulphomucin and sialomucin was found
in the bronchial glands (Wheeldon et al., 1976). The ferret submucous glands contained predominantly neutral
mucins, and scattered between these cells containing
sulphated mucins and sialidase-labile and sialidaseresistant sialomucins (Robinson et al., 1986). The human
tracheobronchial submucous glands contain various
types of sulphomucins and sialomucins, also contain
some neutral mucins (Lamb and Reid, 1972). In addition
to mucins, tracheobronchial serous cells in glands of
man secrete a number of antimicrobial and immunological products, and these are likely to play important roles
in healthy, as well as diseased states (Thompson et al.,
1995; Finkbeiner, 1999).
In the yak bronchial tree, the mucosubstances produced by surface mucus-producing cells exhibited both
acidic and mixed mucosubstances, and the present observation is in agreement with observations made in
other mammalian species, including the camel (Raji and
Naserpour, 2007), goat (Kahwa and Purton, 1996), sheep
(Mariassay et al., 1988), Rhesus monkey (Plopper et al.,
1984) and man (Spicer et al., 1983). However, in buffalo
lung there were no goblet cells (Singh and Mariappa,
1981). The histochemistry of mucosubstances in the tracheobronchial tree of the yak similar to that observed in
some mammalian species, such as sheep (Mariassay
et al., 1988), pig (Jones et al., 1975) and one-humped
camel (Raji and Naserpour, 2007) in which neutral
mucosubstances were seen to predominate, but in adult
Rhesus monkey (Plopper et al., 1989) and goat (Kahwa
and Purton, 1996) the acidic mucosubstances were present in vast majority of surface goblet cells in trachea
and proximal bronchi. But among the carnivores, Wheel-
don et al. (1976) found sulphated and neutral mucin
were the predominant mucosubstance in the epithelial
goblet cells of dog with hardly any sialomucin. The cat
bronchial tree contained mostly sulphated mucin with a
very small amount of sialidase-resistant sialomucin
(Gatlagher et al., 1975). In ferret tracheal goblet cells,
as well as in the bronchi and larger bronchioles, contained sulphated mucins, only a smaller proportion of
the goblet cells showed sialidase-labile and sialidase-resistant sialomucins (Robinson et al., 1986). Goblet cells
in manhad been demonstrated to contain neutral, sialylated, and sulphated sugars (Kim and Jeffery, 1997; Kim
et al., 1997). In the tissue sections of lung, mucous cell
with granules were stained purple with toluidine blue
(Figs.2F, 3F), Granules in serous cell would not be
stained in such manner. This was probably an indication
that two different types of granules in two different
kinds of cells. However, other investigators have shown
metachromatasia of toluidine blue or azur A in both mucous and serous cells, which they claimed distinguished
between sialomucin and sulphomucin (Tock and Tan,
1969; Lamb and Reid, 1970).
From this investigation, we concluded that histochemical nature and ultrastructural characteristics of mucous
cells in the respiratory epithelia and submucosal glands
of yak’s lungs were basically similar to those of other
domestic animals. Though certain differences and variables were observed in each species, the discrepancies
may be due to mutable environmental conditions, e.g. alpine, hypoxia, and cold climate, as well as dissimilarity
in the use of histochemical techniques.
The authors thank with deep and sincere appreciation
for the editorial assistance provided by H. C. Dung,
Ph.D., a retired professor of anatomy, University of
Texas Health Science Center at San Antonio, San Antonio City, Texas, USA, also the farmers for the help with
animal specimen and Yanyu He in Laboratory Center of
Gansu Agricultural University for the technical support.
Basbaum CB. 1986. Regulation of airway secretory cells. Clin Chest
Med 7:231–237.
Basbaum CB, Jany B, Finkbeiner WE. 1990. The serous cell. Annu
Rev Physiol 52:97–113.
Borthwick DW, West JD, Keighren MA, Flockhart JH, Innes BA,
Dorin JR. 1999. Murine submucosal glands are clonally derived
and show a cystic fibrosis gene-dependent distribution pattern.
Am J Respir Cell Mol Biol 20:1181–1189.
Choi HK, Finkbeiner WE, Widdicombe JH. 2000. A comparative
study of mammalian tracheal mucous glands. J Anat 197(Part
Dalen H. 1983. An ultrastructural study of the tracheal epithelium
of the guinea-pig with special reference to the ciliary structure.
J Anat 136:47–67.
Finkbeiner W. 1999. Physiology and pathology of tracheobronchial
glands. Respir Physiol 118:77–83.
Gatlagher JT, Kent PW, Passatore M, Phipps RJ, Richardson PS.
1975. Composition of tracheal mucus and its secretion in the cat.
Proc R Soc Lond 192:49–56.
George JA, Nishio SJ, Cranz DL, Plopper CG. 1986. Carbohydrate
cytochemistry of rhesus monkey tracheal submucosal glands.
Anat Rec 216:60–67.
He J-f, Yu SJ, Cui Y. 2009. Characteristics of lung structure in different age plateau yak. acta veterinaria et zootechnica sinica
Jeffery PK. 1983. Morphologic features of airway surface epithelial
cells and glands. Am Rev Respir Dis 128:S14–S20.
Jeffery PK, Li D. 1997. Airway mucosa: secretory cells, mucus and
mucin genes. Eur Respir J 10:1655–1662.
Jones R, Baskerville A, Reid L. 1975. Histochemical identification of
glycoproteins in pig bronchial epithelium J Pathol 98:213–229.
Kahwa CKB, Purton M. 1996. Histological and histochemical study
of epithelia respiratory tract in adult goat. Small Ruminant Res
Kennedy AR, Desrosiers A, Terzaghi M, Little JB. 1978. Morphometric and histological analysis of the lungs of Syrian golden
hamsters. J Anat 125:527–553.
Kim KC, Jeffery PK. 1997. Airway mucus. Eur Respir J 10:1438.
Kim KC, McCracken K, Lee BCea. 1997. Airway goblet cell mucin:
its structure and regulation of secretion. Eur Respir J 10:
Lamb D, Reid L. 1970. Histochemical and autoradiographic investigation of the serous cells of the human bronchial glands. J Pathol
Lamb D, Reid L. 1972. Quantitative distribution of various types of
acid glycoprotein in mucous cells of human bronchi. Histochem J
Lev R, Spicer SS. 1964. Specific staining of sulphate groups with
alcian blue at low Ph. J Histochem Cytochem 12:309.
Mariassay AT, Plopper CG. 1983. Tracheobronchial epithelium of
the sheep: I. Quantitative light-microscopic study of epithelial cell
abundance, and distribution. Anat Rec 205:263–275.
Mariassay AT, Plopper CG. 1984. Tracheobronchial epithelium of
the sheep: II. Ultrastructural and morphometric analysis of the
epithelial secretory cell types. Anat Rec 209:523–534.
Mariassay AT, St George JA, Nishio SJ, Plopper CG. 1988. Tracheobronchial epithelium of the sheep: III. Carbohydrate histochemical and cytochemical characterization of secretory epithelial cells.
Anat Rec 221:540–549.
McCarthy C, Reid, L. 1964. Acid mucopolysaccharide in the bronchial tree in the mouse and rat. Qu J Exp Physiol 49:81–84.
McManus JFA. 1948. Histological and histochemical uses of periodic
acid. Stain Technol 23:99–108.
Mowry RW. 1956. Alcian blue techniques for the histochemical
study of acidic carbohydrates. J Histochem Cytochem 4:407–408.
Ohtsuka R, Doi K, Itagaki S. 1997. Histological characteristics of
respiratory system in Brown Norway rat. Exp Animals 46:
Okamura H, Sugai N, Kanno T, Shimizu T, Ohtani I. 1996. Histochemical localization of carbonic anhydrase in the trachea of the
guinea pig. Histochem Cell Biol 106:257–260.
Pack RJ, Al-Ugaily LH, Morris G, Widdicombe JG. 1980. The distribution and structure of cells in the tracheal epithelium of the
mouse. Cell Tissue Res 208:65–84.
Plopper CG, George JA, Nishio S, Etchison JR, Netfesheim P. 1984.
Carbohydrate cytochemistry of tracheobronchial airway epithelium of the rabbit. J Histochem Cytochem 32:209–218.
Plopper CG, Heidsiek JG, Weir AJ, George S, Hyde DM. 1989. Tracheobronchial epithelium in the adult Rhesus monkey: a quantitative histochemical and ultrastructural Study. Am J Anat
Raji AR, Naserpour M. 2007. Light and electron microscopic studies
of the trachea in the One-Humped camel (Camelus dromedarius).
Anat Histol Embryol 36:10–13.
Reid L. 1960. Measurement of the bronchial mucous gland layer: a
diagnostic yardstick in chronic bronchitis. Thorax 15:132–141.
Robinson NP, Venning L, Kyle H, Widdicombe JG. 1986. Quantitation of the secretory cells of the ferret tracheobronchial tree.
J Anat 145:173–188.
Rogers AV, Dewar A, Corrin B, Jeffery PK. 1993. Identification of
serous-like cells in the surface epithelium of human bronchioles.
Eur Respir J 6:498–504.
Shimura S. 1990. Methods for the morphological study of tracheal
and bronchial glands. In: Gil J, editor. Models of Lung Disease:
Microscopy and Structural Methods. Florida: CRC Press. p
Singh K, Mariappa D. 1981. Histological studies of the conducting
and the respiratory division of the buffalo lung. Indian Vet J
Spicer SS, Schulte BA, Chakrin LW. 1983. Ultrastructural and histochemical observations of respiratory epithelium and gland. Exp
Lung Res 4:137–156.
Staley MW, Trier JS. 1965. Morphologic heterogeneity of mouse
Paneth cell granules before and after secretory stimulation. Am J
Anat 117:365–384.
Steiger D, Hotchkiss J, Bajaj L, Harkema J, Basbaum C. 1995. Concurrent increases in the storage and release of mucin-like molecules by rat airway epithelial cells in response to bacterial
endotoxin. Am J Resp Cell Mol 12:307–314.
Takenaka S, Heini A, Ritter B, Heyder J. 1996. Morphometric evaluation of bronchial glands of beagle dogs. Toxicol Lett 88:
Thompson AB, Robbins RA, Romberger DJea. 1995. Immunological
functions of the pulmonary epithelium. Eur Respir J 8:127–149.
Tock EP, Tan NT. 1969. A histochemical study of the mucins of the
adult human nasopharynx. J Anat 104:81–92.
Wheeldon EB, Pnue HM, Bassz RG. 1976. A histochemical study of
the tracheobronchial epithelial mucosubstances in normal dogs
and in dogs with chronic bronchitis. Folia veterinaria Latina
Widdicombe JH, Chen LL, Sporer H, Choi HK, Pecson IS, Bastacky
SJ. 2001. Distribution of tracheal and laryngeal mucous glands in
some rodents and the rabbit. J Anat 198:207–221.
Widdicombe JH, Pecson IS. 2002. Distribution and numbers of mucous glands in the horse trachea. Equine Vet J 34:630–633.
Wilson DW, Plopper CG, Hyde DM. 1984. The tracheobronchial epithelium of the bonnet monkey (macacaradiata): a quantitative ultrastructural study. Am J Anat 171:25–40.
Yeadon M, Price RC, Payne AN. 1995. Allergen-induced glycoconjugate secretion in guinea pig trachea in vivo: modulation
by indomethacin, BW B70C and ZD-2138. Pulm Pharmacol 8:
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ultrastructure, epithelium, respiratory, observations, gland, yak, grunniens, bos, histochemical
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