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Morphological and morphometric changes in the ovaries of white-footed mice (Peromyscus leucopus) following exposure to long or short photoperiod.

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THE ANATOMICAL RECORD 205:13-19 (1983)
Morphological and Morphometric Changes in the Ovaries
of White-footed Mice (Peromyscus leucopus)
Following Exposure to Long
or Short Photoperiod
KATHARINA SPANELBOROWSKI, LARRY J. PEITERBORG, AND RUSSEL J.
REITER
Department of Anatomy, The University of Teras Health Science Center at Sun Antonw,
San Antonw, TX 78284
ABSTRACT
Two experiments were carried out with a total of 36 white-footed
mice (Peromyscus leucopus) exposed to either long (LP) or short (SP) photoperiod
for six weeks. Ovaries and uteri were weighed. Serial sections of the ovaries were
processed for light microscopy. The total number of the interstitial gland cells,
preantral and antral follicles with early and advanced stages of atresia as well
as corpora lutea, was determined.
Uteri from LP mice weighed significantly more than those from SP mice in
both experiments. In contrast, the weight of ovaries from LP and SP animals only
differed significantly in one experiment; this experiment also produced no obvious
changes in the total number of corpora lutea. While interstitial gland cells of LP
ovaries were hypertrophic and appeared mature, the interstitial gland cells of SP
ovaries were of the degenerating cell type, The total number of follicles as well
as their mean follicular diameters were higher in LP animals in comparison with
SP animals. In addition, the percentage of antral follicles were increased and
there were fewer signs of advanced stages of atresia in the LP group. It is suggested
that the changes of the interstitial gland cell morphology combined with alterations of follicular growth during LP or SP appear to support intensified follicular
growth.
While the importance of the testicular interstitial cells of Leydig for spermatogenesis is
well known, little information is available on
the significance of the interstitial gland cells
in the ovary. Ovarian interstitial gland cells
may be involved in the maintenance of pregnancy (Kraicer et al., 1971), the expression of
secondary sex characters (Mossman and Duke,
1973),or the support of follicular growth. The
latter possibility is derived from new knowledge concerning steroidogenesis in the ovary.
It has been shown in hypophysectomized immature rats and with cultured rat theca and
granulosa cells that androgens are produced
by LH-stimulated cells (Armstrong and Papkoff, 1976 Fortune and Armstrong, 1977,1978).
These androgen-producing cells appear to belong to the interstitial gland cells as well as
the theca (Dorrington and Armstrong, 1979).
Androgens are then aromatized to estrogens
by granulosa cells and thereby increase follic-
ular responsiveness to gonadotropins (Richards, 1980).
The possibility of follicular growth being dependent upon the interstitial gland cells was
tested in the white-footed mouse, Peromyscus
leucopus, during long and short photoperiodic
exposure. This small North American rodent
is known to be highly sensitive to the inhibitory effects of short photoperiods on reproduction (Lynch, 1973;Petterborg and Reiter, 1981).
In photosensitive species, i t has been shown
that the number of preantral and antral follicles increases or decreases during long or short
photoperiods, respectively (Reiter and Johnson, 1974; Petterborg et al., 1981).The purpose
of the following study was to determine if
h i v e d July 15, 1982; accepted October 11, 1982
K.S.B.’spermanent address is: Abteilung fir Klinisehe Morphologie
der Universiut ULM, Postfach 4066, D7900 ULM, FRG.
0003-276X/83/2051-0013$02.500 1983 ALAN R. LISS, INC.
14
K. SPANEL-BOROWSKI, L.J. PETTERBORG, AND R.J. REITER
changes in follicular growth are correlated with
morphologicalchanges in the interstitial gland
cells in ovaries from mice exposed to either
long or short photoperiods.
MATERIALS AND METHODS
Thirty-six young adult, laboratory-reared
white-footed mice (Peromyscus leucopus) were
housed three to five per clear plastic cage in
an air-conditioned(22 -C 2”C),windowless room.
They were supplied with food (Wayne Lab-Blox)
and water ad libitum. Two identical experiments were conducted during the months of
September and October. For experiment 1, 16
animals were available, while for experiment
2,20 animals were used. In each study half of
the animals were kept in long photoperiods,
LP (LD 16:8, lights on a t 06:OO h) with the
remainder being maintained under short photoperiods, SP (LD 8:16, lights on at 06:OO h).
The LD cycles were automatically controlled.
At the end of six weeks, the animals were killed
by decapitation; both ovaries and the uteri were
removed, weighed and tissues were fixed in
Bouin’s solution. Usually one ovary was fured
with the exception of three animals in experiment 2, where both ovaries were taken. The
processing of the tissue was done by common
histological methods. The ovaries were sectioned (thickness of 7 pm); tissues were stained
with hematoxylin and eosin.
Evaluation of the Ovaries
Every third section out of 120 serial sections
from each ovary was examined for changes in
the interstitial gland cells, the follicles and the
corpora lutea. For the interstitial gland cells,
the number of nuclei was determined for an
area of 100 Fm2 with an ocular grid at an objective magnification of 100 X . Nuclei of endothelial cells were excluded. The area analyzed had to be free of follicles or prominent
vessels. For the follicles, the classification of
primordial, preantral and antral follicles was
used (Bloom and Fawcett, 1975). Only preantral (mean diameter more than 100 pm) and
antral follicles were counted. Since the mean
nuclear diameter of the oocyte nucleus in this
species is about 20-25 Fm, repetition was
avoided by counting follicles only when the oocyte nucleus was cut. Counting the follicles of
some ovaries on two different days gave similar numbers. The follicles were subdivided into
two stages: Stage I contained no or early signs
of atresia (S1:
slight deformation of the oocyte,
a few pyknotic granulosa cells) and stage I1
with advanced signs of atresia (SZ:
pronounced
deformation or necrosis of the oocyte, high
number of pyknotic granulosa cells, intercellular loosening of the granulosa layer). The
general morphological changes of atresia have
been described in detail elsewhere (Spanel-Borowski, 1981). The total number of preantral
and antral follicles as well as the percentage
of preantral and antral follicles with their stages
of atresia was determined. For each follicle,
two diameters,perpendicular to each other, were
determined with an ocular micrometer a t an
objective magnification of 10 X ; these measurements were averaged for the mean follicular diameter. Corpora lutea were counted in
every 12th section; thus, corpora lutea were
counted in 10 sections from each ovary. The
mean number of corpora lutea in these 10 sections was taken as the total number of corpora
lutea in a given ovary. Student’s t test was used
to detect significant differences in the various
parameters between the two photoperiodic
groups.
RESULTS
The mean weight of the uteri taken from
mice kept in LP was significantly greater than
that from SP animals (Table 1). This held true
for both experiments. In contrast, there was a
significant difference in the mean weights of
the ovaries from the two photoperiodic groups
only in experiment 2; this might be explained
by the differences in the total number of corpora lutea (Table 2). While animals in experiment 1 had ovaries which contained similar
numbers of corpora lutea in both photoperiods,
in experiment 2 the number of corpora lutea
differed significantly between the two groups.
The ranges of the total number of corpora lutea
as well as the ranges of ovarian weights showed
that ovaries from animals of both photoperiods
varied widely (Tables 1 and 2).
Interstitial Gland Cells
The interstitial gland cells of ovaries from
mice kept in LP had a hypertrophic appearance
and appeared metabolically active (Fig. 1). The
hypochromatic nuclei of these cells were vesicular in shape, and there was abundant cytoplasm. The cells were seen lying in clusters
or in vertical cords, often close to capillaries.
The cells in these ovaries were termed “mature
interstitial cell types” in accordance with a terminology applied to the interstitial gland cells
of the rabbit ovary (Davis and Broadus, 1968).
The interstitial gland cells were completely
different in structure in ovaries from animals
kept in SP (Fig. 2); the latter were atrophic in
OVARIAN CHANGES IN WHITE-FOOTED MICE AFTER LP/SP
15
TABLE 1 . Weights of ovaries and uteri of adult white-footed mice
exposed to long (LP)and short (SP) photoperwda for siz weeks
Number of
Photoperiod Experiment animals
LP
SP
1
a
2
10
1
8
2
10
Ovarian
weight
(rng)
14.3 5 3.0
(8.1-16.5)
20.4 r 8.9*
(10.6-42.5)
11.0 2 7.5
(2.0-20.2)
8.2 -t 4.3
(3.5-15.8)
Uteran
weight
(mg)
72.0 2 39.8*
(21.9-147)
44.0 -e 16.6**
(14.6-67.3)
13.9 5 7.3
(4.7-26.9)
11.1 2.7
(6.6-14.3)
*
Data are means 2 SD; ranges in parentheses.
*p < 0.01; **p < 0.001compared with SP of the same experiment.
TABLE 2. Total number of corpom lutea in adult whitefooted mice exposed to long (LP)and short (SP)
photoperwds for six weeks
Experiment
Number of
ovaries
1
8
2
13
Corpora lutea"
LP
SP
5.0 k 1.9
(2-7)
6.2 2 1.9*
(3-9)
4.5 ? 2.1
(0-7)
4.1 r 2.4
(0-7)
Data are means 2 S D ranges in parentheses.
Tounted and averaged in 10 out of 120 serial sections.
*p < 0.05, compared with SP of the Bame experiment.
appearance, but irregularly shaped, hyperchromatic nuclei, sparse cytoplasm and no particular cell arrangement could be discerned.
The cells in these ovaries were classified as
"degenerating" cells (Davis and Broadus, 1968).
Because of the size difference,fewer nuclei were
counted per 10 pm2in LP mice than in SP mice
(Table 3). These differences were highly significant (p < 0.001). When viewed under low
magnification, the ovarian cortex appeared hypochromatic in samples from animals maintained in LP; the boundary of the medulla was
not well marked. In sections from animals kept
in SP the cortex was hyperchromatic and could
be easily distinguished from the medulla.
Follicles
More preantral and antral follicles were present in LP ovaries in comparison to ovaries
from SP females; however, only for experiment
2 was the difference statistically significant
(Table4). In experiment 1,antral follicles were
present in only 37% of the ovaries from SP
animals, while in the second study antral follicles were found in only 16% of the ovaries
from SP-exposed mice. Ovaries after exposure
to LP showed more early stages of atresia in
comparison with ovaries from animals kept in
SP; this was statistically significant (p < 0.02)
in experiment 2. Conversely, advanced stages
of atresia were increased after SP. The differences were not significant in both photoperiodic groups since the values of each follicular
category displayed high ranges. The largest
mean follicular diameters were found in ovaries from animals aRer treatment with LP;
many of these contained an antrum. The smaller
follicular size in SP ovaries was related to the
prevalence of preantral follicles. Follicular size
for the two photoperiodic groups differed significantly only in experiment 2.
DISCUSSION
This study demonstrates that exposure of
white-footed mice to long photoperiodic (LP)
conditions supports the growth of antral follicles and stimulates the maturation of interstitial gland cells in the ovaries. Six weeks
exposure to short photoperiods (SP) does not
appear to be able to completely halt the development of antral follicles. It is possible that
more than six weeks of short day treatment
would be more effective in suppressing follicular growth. If prolonged SP treatment would
eventually cause the antral follicles to disappear completely is not known. In Syrian hamsters a few antral follicles still remain after
eight weeks of light deprivation (Reiter and
Johnson, 1974).In the present investigation,
16
K. SPANEL-BOROWSKI, L.J. PETTERBORG, AND R.J. REITER
Fig. 1. Interstitial gland cells in the ovary of the whitefooted mouse exposed to long photoperiod for six weeks. The
mature cell type appears. x 860.
Fig. 2. Interstitial gland cells in the ovary of the whitefooted mouse exposed to short photoperiod for six weeks.
The degenerating cell type is apparent. x 860.
17
OVARIAN CHANGES IN WHITE-FOOTED MICE AFTER LP/SP
TABLE 3. Number of interstitial gland cells in ouaries of adult white-footed
mice exposed to Eong (LPI or short photoperiods @Pi for sir weeks
Experiment
Number of
ovaries
1
8
2
13
Number of interstitial gland cells per 100 *ma
LP
SP
388 f 74
(322-611)
384 t 57
(286493)
212 f 41*
(136-265)
207 f 51*
(127-283)
Data are means T S D ranges in parentheses.
.One area evaluated per ovary.
*p < 0,001,compared with SP of the same experiment
it is possible that ovulation occurs and new
corpora lutea develop after six weeks exposure
to SP. This helps to explain the lack of a statistical significancebetween the mean ovarian
weights and the total number of follicles in
experiment 1; a greater ovarian function is assumed for experiment 1 because more antral
follicles are found in these ovaries in comparison with experiment 2. In addition, persistence of corpora lutea for several weeks, which
is known for the SP animals (Margolis and
Lynch, 1981), may be longer in experiment 1
and therewith also contribute to the similar
ovarian weights in the two groups of the first
study. Since the animals were reared in a windowless room under a consistent photoperiod
and since both experiments were done at the
same time of the year, it is unlikely that the
observed differences are due to a seasonal effeet. SP,however, significantlyaltered the mean
ovarian weight and the total number of folli-
cles in experiment 2. Among the changes observed in LP ovaries compared with SP ovaries
were: A higher total number of follicles, a
greater percentage of antral follicles, a decline
of advanced stages of follicular atresia as well
as a decrease in the total number of corpora
lutea. The increase in follicular growth is in
accordance with previous reports where only
estimates of these changes were noted (Reiter
and Johnson, 1974; Petterborg et al., 1981).
Statistical significance has not been apparent
in each follicular category of this study. Acomplete investigation of both ovaries might be
necessary to obtain always significant values.
It is known that the right ovary can vary from
the left one in the total number of follicles to
a large degree (Green and Zuckerman, 1951).
The method applied to count the total number
of corpora lutea is not valid in all aspects because the ratio of the investigated tissue block
to the whole ovary changes for a large ovary
TABLE 4 . Total number of ouarian follicles, percentage of antml follicles with early (Sd and advanced (SZ,stages of
atresia and largest mean follicular diameters in the adult white-footed mice exposed to either long (LP) or short (SP)
photoperiods for sir weeks
Photoperiod Experiment
Number
of
ovaries
Total
number of
follicles'
s1
Percent of antral follicles" Largest mean
follicular
diameter
SI +
(pm)
sz
sz
~~~
LP
SP
1
8
2
13
1
8
2
13
30 f 11
(21-51)
31 f 14***
(13-52)
21 f 9
(7-32)
16 6
(3-25)
*
4.9 2 2.9
(0-8.7)
2.9 f 3.0**
(0-8.7)
2.2 f 3.3
(0-8.7)
0
4.5 k 5.7
(0.0-14.8)
1.4 2 1.7
(0-4.3)
2.2 2 2.5
(0-6.3)
1.2 f 3.2
(0-11.1)
Data are means T SD; ranges in parenthesee.
.Counted in every third section out of 120 serial sections; primordial follicles excluded.
*p < 0.05; **p < 0.02; ***p < 0.01; tp i0.001. compared with SP of the mme experiment.
9.4 f 3.6*
(5.4-14.8)
4.3 k 3.8
(0-10.9)
4.3 f 4.6
(0-13.0)
1.2 f 3.2
(0-1 1.1)
381 e 111
(275-525)
436 f 104t
(275-550)
301 e 27
(175-245)
253 f 27
(188-290)
18
K. SPANEL-BOROWSKI, L.J. PETTERBORG, AND R.J. REITER
in comparison with a small ovary. Yet the error
is low, since existing or missing differences in
the total number of corpora lutea are confirmed
by existing or missing differences in the ovarian weight of both experiments.
This report compares for the first time the
appearance of the interstitial gland cells in long
and short photoperiod exposed animals. The
interstitial gland cells of the white-footed mouse
seem to be highly sensitive to photoperiodic
manipulations. LP induced hypertrophy and
maturation of the interstitial gland cells, while
SP caused atrophy of these cells. The structure
of the interstitial gland cells after SP reminds
one of the so-called “deficiency-cells”in the rat
ovary; they appear in the interstitial cortical
tissue of senile rats or after hypophysectomy
of fertile rats and can be stimulated to full size
by exogenous LH (Carithers and Green, 1972;
Crumeyrolle-Arias et al., 1976).In this context
it is of interest that in the dog ovary the mature
cell type can be provoked and its number increased after a 1200 R whole-body x-irradiation (Spanel-Borowski and Calvo, 1982). The
mechanism of maturation is probably related
to increases in hypothalamic function during
long days and decreases during short day exposure (Reiter, 1980).Presumably, during long
days the pituitary is stimulated by increased
amounts of luteinizing hormone releasing hormone (LH-RH) and serum levels of LH increase. A primary target of LH in the ovary
are the interstitial gland cells (Dorrington and
Armstrong, 1979). The ovarian changes attributed to photoperiodic manipulations may
also involve prolactin, since in the male golden
hamster (Bex et al., 19781, the dwarf mouse
(Bohnet and Friesen, 19761, and the male rat
(Zipf et al., 1978)prolactin, in conjunction with
LH, produces the maximal response in the interstitial gland cells. Short day exposure, because of its action on the pineal gland, is known
to depress both LH and prolactin in a number
of rodent species (Reiter, 1980) with the exception of female Syrian hamsters which usually show an increase in the LH levels (Reiter
and Johnson, 1974). In contrast to the whitefooted mouse, the ovary of the Syrian hamster
responds to light restriction with a marked hypertrophy of the interstitial gland cells.
Ten years ago, the histological findings concerning the maturation of the intemtitial gland
cells and the increase of follicular growth in
animals kept in LP would have been interpreted to be two separate events. Today, steroidogenesis is considered to be a function of
the non-follicular cortical tissue since it is
seemingly responsible for the production of androgens, while the granulosa cells are involved
with the aromatization of the androgens to estrogens (Leung and Armstrong, 1980). An interaction of the interstitial gland cells with the
follicles is supported by the observations of this
study. It appears that the interstitial gland
cells may support follicular growth. This possibility is strengthened by the report of Guraya
(1978) that the mature cell type predominates
in some species at the time of ovulation. The
supportive action of the interstitial gland cells
probably relates to the fact that the cells predominantly produce androgens. Recent data
suggest that the interstitial gland cells are the
main site of androgen production for the ovary,
at least in the rat (Armstrong and Papkoff,
1976; Magoffin et al., 1981) and in the human
(McNatty et al., 1979; Dennefors et al., 1980).
In the rabbit (Guraya, 1978) and in the golden
hamster (Taya et al., 1980) progesterone, in
addition to androgens, may be produced. Presumably, the capacity of interstitial gland cells
to secrete different amounts of estrogens, progestins and androgens changes according to
their exposure to FSH and LH (McNatty et al.,
1979). This finding may also explain why in
female hamsters after light deprivation, and
in spite of their hypertrophied interstitial gland
cells, the number of preantral and antral follicles is reduced (Reiter and Johnson, 1974).
Since blood levels of FSH are depressed and
LH levels are normal or increased, the hypertrophied interstitial gland cells of female Syrian hamsters are probably secreting progestins. The function of ovarian interstitial gland
cells can be similar to that of the interstitial
cells of Leydig in the testis which are known
to be important for spermatogenesis. In the
white-footedmouse it has been shown that more
testosterone is produced in animals after exposure to LP (Petterborg and Reiter, 1981).
Thus, it is suggested that the interstitial gland
cells of the ovary of Peromyscus leucopus appears as a local promoter of intensified follicular growth during long day exposure.
ACKNOWLEDGMENTS
We gratefully acknowledge the secretarial
help of Mrs.Nancy Elms as well as the critical
and capable reading of the manuscript by Dr.
E.G. Rennels. This study was supported by a
grant from the DFG (Deutsche Forschungsgemeinschaft) to K.S.B., and by N.S.F. grant
no. PCM 8003441 to R.J.R.
OVARIAN CHANGES IN WHITE-FOOTED MICE AFTER LP/SP
19
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