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Postnatal development of the duct system in the mouse parotid gland.

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THE ANATOMICAL RECORD 217:391-394 (1987)
Postnatal Development of the Duct System in the
Mouse Parotid Gland
MASAHARU DOMON AND TOHRU KURABAYASHI
Department of Dental Radiology, Tokyo Medical and Dental University, 1-5-45 Yushima,
Bunkyeku, 113 Tokyo, Japan
The morphology of the parotid gland in adult mice is mouse strainABSTRACT
specific. C57BL/6 and C3WHe strains of mouse are representatives of two types of
the morphology identified previously. The postnatal development of such morphologic differences was investigated by sialography of excised glands of these strains
of mouse. It was observed that the mouse strain-dependent morphological characteristics were already present a t birth, except for the branching pattern of the peripheral duct system, which became differentiated at 3 weeks of age. These results
indicate that the C3H/He mouse-specific branching pattern of the peripheral ducts
reflects the profile of matured secretory units and ducts, and that the C57BL/6
mouse-specific pattern resembles that of a n immature C3WHe mouse.
Sialograms of the adult mouse parotid glands are characterized by the presence of the accessory lobe, the shape
of the major lobe, and the branching pattern of the
peripheral duct system, which are mouse strain-dependent (Domon and Shiga, 1986).The question arises as to
the stage of mouse development when such characteristics are expressed. The morphogenesis of the parotid in
the rodent is initiated late in prenatal life. At the time
of birth, the parotid is still very immature, consisting of
a canalized, branching duct system and solid terminal
buds (reviewed by Young and van Lennep, 1978).During
early postnatal development of the rat parotid gland,
increases in the number of cells and amylase activity
are associated with increases in the numbers of secretory units and ducts (Redman and Sreebny, 1970, 1971).
Thus, one might predict that the strain-dependent morphologic differences in the mouse parotid gland are incompletely developed at birth.
To investigate this problem, sialographic studies were
carried out on the excised parotids of C57BL/6 and C3W
He postnatal mice a t representative intervals from 3
days to 9 weeks of age. It was confirmed from these
studies that the strain-dependent differences in the peripheral duct system of the gland were developed at 3
weeks of the postnatal life of the mouse.
Sialography
The method of sialography of the mouse was previously described (Domon and Shiga, 1986). Briefly, Stensen’s duct was transversely cut and a stainless steel
needle of 250 pm diameter was inserted, through which
X-ray contrast medium of barium sulfate sol was infused. The glands were then excised, weighed, and radiographed by soft X-rays a t 10 kVp or 25 kVP. Glass
capillaries were used instead of the needle for infusion
of the small Stensen’s ducts up to 3 weeks of age. By use
of a glass microelectrode puller (Model PN-3, Narishige
Scientific Inst. Lab., Tokyo), the capillaries were made
from 1.0 mm diameter Pyrex glass tubes with tips of 50125 pm diameters, which were matched to the sizes of
Stensen’s ducts. The capillaries were connected to a
microinjector (Model IM-3, Narishige Scientific Inst.
Lab., Tokyo) whose pressure was controlled by mineral
oil (Sigma, St. Louis, MO) by the use of micrometer
screw. The amount of infused X-ray contrast medium
was 0.1 ~1 per 3 mg wet-weight gland.
The mean of the gland weight for each age group of
mice was calculated as follows. When a single gland
weight was measured from a single mouse, the weight
was used as the data for the mouse. When a pair of the
glands of a single mouse were weighed, their averaged
MATERIALS AND METHODS
weight was used as the data for the mouse. The mean
and SEM were based on these data for mice of the age
Animals
Two inbred strains of mice, C57BL/GNCrj and C3W group.
HeNCrj (Charles River Japan, Atsugi, Kanagawa), were
RESULTS
used at day 0, day 3, 1 week, 3 weeks, 6 weeks, and 9
Growth of the Parotid Gland
weeks of age. The date of birth was designated as day 0.
Both sexes of animals were used until weaning at 3 The wet weight of the gland increased at a faster rate
weeks of age, after which only male animals were used. than body weight during the first 3 weeks of age in both
Whole Mount Preparation
The excised parotid from a C 3 W e mouse a t day 0
was fixed in acetone €or 48 hours and then stained with
Mayer’s hematoxylin. The stained gland was mounted
on a glass micro slide in 1 : l glycerol-water.
0 1987 ALAN R. LISS, INC.
Received August 12, 1986; accepted November 19, 1986.
Address reprint requests to Dr. M. Domon, Tokyo Medical and
Dental University, Department of Dental Radiology, 1-5-45 Yushima,
Bunkyo-ku, 113Tokyo, Japan.
392
M. DOMON AND T. KURABAYASHI
TABLE 1. Increases in body weight' and wet weight of the parotid gland2 in the
postnatal mouse
Age
(weeks)
Day 0
Day 3
1
2
3
6
9
C57BLI6
Body weight
Gland weight
(€9
(mg)
1.3 f 0.06 (4)
2.8 f 0.2 (5)
4.7 + 0.2 (11)
7.1 & 0.3 (10)
8.6 & 0.7 (11)
20.9 f 0.3 (3)
23.7 & 0.4 (3)
IThe values a r e means
'The values a r e means
"'Not measured
*
1.4 0.2 (7)
2.3 0.2 (17)
7.2 f 0.5 (16)
17.2 1.2 (18)
35.2 + 3.7 (6)
39.4 f 1.9 (6)
Body weight
(g)
C3HIHe
Gland weight
(mg)
1.3 f 0.05 (6)
2.5 f 0.2 (10)
6.3 k 0.3 (20)
10.0 f 0.3 (16)
12.3 k 0.7 (21)
24.4 f 0.7 (10)
27.0 f 0.5 (9)
*
1.0 f 0.1 (15)
3.7 f 0.3 (28)
10.2 k 0.5 (26)
19.8 f 1.3 (35)
36.6 f 1.3 (16)
36.8 i 0.9 (14)
SEM's, and the numbers in parentheses indicate t h e numbers of mice.
SEM's and t h e numbers i n parentheses indicate t h e total numbers of glands.
the C57BL/6 and C3WHe mouse, as shown in Table 1.
The growth of the mouse parotid gland has not been
reported previously. Such relationships are similar to
those reported in rats (Redman and Sreebny, 1971; Klein,
1982).
Shape of the Gland
X-ray contrast medium, many peripheral ducts were not
infiltrated by the contrast medium during the period
(data not shown). At 3 weeks of age the C3WHe mousespecific peripheral duct pattern was developed in the
C3WHe mouse (Fig. 2B4), but not in the C57BL/6 mouse
(Fig. 2A4). At 3 weeks of age or a t later stages, the
number of branches in the duct systems rapidly increased and a t 6 weeks of age the sialograms were similar to those of adult mice of the respective strains (data
not shown).
Thus, the branching patterns of the peripheral duct
systems were distinguished between C3WHe and
C57BL/6 mice a t 2 to 3 weeks of age. The branching
patterns for adult C57BL/6 mice remained similar to
those for immature mice, while those for C3WHe mice
underwent further development.
A photograph of a whole mount of the parotid of a
C3WHe mouse a t day 0 is shown in Figure 1. The
excretory ducts including the major excretory duct,
Stensen's duct (the main stem of the parotid tree in the
photograph), were revealed (Young and van Lennep,
1978). In addition, the C 3 M e mouse-specific shape of
the gland was expressed with rounded outlines of the
lobes and the accessory lobe was present at day 0 (shown
by the arrowhead in Fig. 1)(Domon and Shiga, 1986).
The frequencies of the glands with accessory lobes were
DISCUSSION
315, 11/15, and 22/30 for C3II/He mice a t day 0, day 3,
and 1 week of age, respectively, and so showed no ageThe present sialographic results indicate that the
dependency. Pooled data of the frequencies for day 0 to mouse strain-dependent characteristics of the parotid
9-week-old C3WHe mice were 1071141. In contrast, the gland are expressed a t birth, except for the branching
frequency for day 0 to 9-week-old C57BL/6 mice was 1/
71. These results are similar to those for 12-week-old
mice reported previously (Domon and Shiga, 1986).
Development of Peripheral Ducts
The ductal branching pattern of the mature parotid
gland in sialograms is dependent on the strain of mouse.
The pattern for C3WHe mice is characterized by more
numerous excretory ducts, a more dense peripheral duct
system, and smoother transitions in the size of ducts
than that for C57BL/6 mice.
Attempts a t sialography for day 0 mice failed due to
leakage of X-ray contrast medium from excretory ducts.
At day 3 or later the sialography was successful and the
numbers of sialograms taken were the same as the numbers of glands shown in Table 1 for each age group of
mice. The photographs in Figure 2 are representatives
of sialograms of each age group. The C3WHe mousespecific branching of excretory ducts was evident for the
C 3 M e mouse a t day 3, which were more numerous
(Fig. 2Bl) than those of the C57BL/6 mouse (Fig. 2A1).
However, up to 2 weeks of age, the branching patterns
of peripheral ducts of C57BLi6 mice (Fig. 2A1, A2, A3)
and C3WHe mice (Fig. 2B1, B2, B3) were similar with
high contrast for the excretory ducts or with poorly
displayed peripheral duct systems. By microscopic observations of the whole mounts of the glands infused with
Fig 1. Photograph of a whole mount of the parotid gland of a C3W
H e mouse a t birth. The gland was stained with Mayer's hematoxylin.
The main stem of t h e parotid tree is Stensen's duct, and t h e arrowhead
indicates the excretory ducts of a n accessory lobe of the parotid. X23.
Fig. 2. Sialograms of the developing parotids of C57BL/6 (A series) and C3WHe mice (B series). The
photographs were taken of mice at day 3 (Al, Bl), 1 week (A2, BZ), 2 weeks (A3, B3), and 3 weeks (A4, B4)
of age. The main stems of the parotid trees are Stensen’s ducts. At 2 weeks after birth, excretory ducts
were revealed in the sialograms; however, most of the peripheral ducts were not. Al,B1, X 15.0; A2,B2,
~ 1 3 . 5A3,
; ~ 7 . 0B3,
; ~ 7 . 5A4,B4,
;
~7.0.
394
M. DOMON AND T. KURABAYASHI
pattern of the peripheral duct system. The development
of the C3WHe strain-specific pattern of the peripheral
duct requires 2-3 weeks of postnatal life. During this
period, the gland wet weight increases a t a faster rate
than the body weight. This may be due to the immature
stage of development of the parotid gland a t birth, followed by its rapid postnatal growth (Young and van
Lennep, 1978). In fact, the ratio of parotid weight to
body weight increases from 0.05% at day 3 and 1 week
of age to 0.14% or more at 3 weeks (see Table 1).At
weaning, the peripheral duct pattern for the C3H/He
mouse departs from the immature duct pattern; however, that for the C57BL/6 mouse does not.
Studies on rat parotid glands reported by others appear to be relevant to the present work on the mouse.
The rat weaning stagecoincides with maturation of the
greater than 12 months or when ligation of Stensen's
duct blocks the secretory activity of the gland (unpublished data) (Schneyer and Schneyer, 1961).The C57BL/
6 mouse may lack the ability to respond to the function
of the mature acinar cells.
ACKNOWLEDGMENTS
We thank Dr. A.M. Rauth for his critical reading of
the manuscript. This work was partly supported by a
grant-in-aid for science from the Ministry of Education,
Science and Culture, Japan, No. 58440074.
LITERATURE CITED
Domon, M., and Y. Shiga (1986) Sialographic investigations on the
anatomy of mouse parotid glands. Anat. Rec., 214:165-167.
Gabe, M. (1956) Contribution a l'histogenese de glandes salivaires chez
la Souris albinos. Zeitsch. Zellforsch., 4574-95.
Hall, H.D., and C.A. Schneyer (1969) Physiological activity and regulation of growth of developing parotid. Proc. Soc. Exp. Biol. Med.,
131:1288-1291.
Johnson,
~ D.A., L.M.
~ Sreebny,
~ and c~. 0 . Enwonwu
,
(1977) Effect of protein-energy malnutrition and of a powdered diet on the parotid
gland and pancreas of young rats. J. Nutr. 107:1235-1243.
Klein, R.M. (1982) Acinar cell proliferation in the parotid and submandibular salivary glands of the neonatal rat. Cell Tissue Kinet.,
15187-195.
Lawson, K.A. (1970) Morphogenesis and functional differentiation of
the rat parotid gland in vivo and in vitro. J. Embryol. Exp. Morph.,
24:411-424.
Redman. R.S., and L.M. Sreebny (1970)Proliferative behavior of differentiating cells in the developing rat parotid gland. J. Cell Biol.,
463-87.
Redman, R.S., and L.M. Sreebny (1971) Morphologic and biochemical
observations on the development of the r a t parotid gland. Devel.
Biol., 25:248-279.
Redman, R.S., and L.M. Sreebny (1976) Changes in patterns of feeding
activity, parotid secretory enzymes and plasma corticosterone in
developing rats. J. Nutr., 106t1295-1306.
Schneyer, C.A., and H.D. Hall (1969) Growth pattern of postnatally
developing r a t parotid gland. Proc. Soc. Exp. Biol. Med., 130t603607.
SChneyer, C.A., and L.H. Schneyer (1961) Secretion by salivary glands
deficient in acini. Amer. J. Physiol., 201:939-942.
Young, JA and E.W. van L e n n e ~(1978) The M o r ~ h o of
b ~Salivary
Academic, New York.
'
parotid gland in terms Of a great increase in the number
Of Secretory units and ducts, amylase specific activity,
circadian rhythms in cell proliferation (Schneyer and
~ ~ 1 1969;
1 , Redman and Sreebny, 1970, 1971; L
~
1970; Klein, 19821, and secretory enzyme secretion and
storage (Redman and Sreebny, 1976; Schneyer and Hall,
1972). It is disputed whether the uptake of solid food by
the young
is the factor that induces the parotid
maturation (Lawson, 1970). The role of the uptake of
solid food for the gland maturation is supported by the
evidence that liquid diet and powdered food delay acinar
maturation of weaning rats and
atrophy of the
acini in older rats (Hall and Schneyer, 1969; Redman
and Sreebny, 1976; Johnson et al., 1977). To what extent
ductal
is affected by the uptake Of 'lid
food has not been addressed.
not a s thoroughly
investigated as the rat parotid gland, the evidence indicates that the development of the mouse parotid also
matures in conjunction with weaning (Gabe, 1956).
the
Of the C3H/He mouse-specific duct pattern may be related to the maturation of
acinar cell function. This is supported by the observation
that the peripheral duct pattern for C3H/He mice becomes similar to that for the C57BL/6 mouse a t ages
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