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Prevention by pinealectomy of short-photoperiod-induced ultrastructural changes in the hamster harderian gland.

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THE ANATOMICAL RECORD 210:449-452 (1984)
Prevention by Pinealectomy of Short-Photoperiod-lnduced
Ultrastructural Changes in the Hamster Harderian Gland
DENNIS P. DIIORIA
AND
MATHEW J. NADAKAVUKAREN
Biological Sciences Department, Illinois State University, Normal, IL 61 761
ABSTRACT
Harderian gland ultrastructure was examined at biweeky intervals for 16 weeks after either pinealectomy or sham-operation of male and
female hamsters kept in 1L:23D and 14L:10D photoperiods. Female characteristics such as membrane formations and extensive smooth endoplasmic reticulum appeared in the males kept under short photoperiod conditions. Similarly,
male characteristics such as the tubular clusters appeared in the glands of
females kept in the short photoperiod. When male and female hamsters were
pinealectomized and exposed to the short photoperiod, the glands in each sex
retained the characteristics typical of that sex. Atrophy of the testes and uteri
was also observed in the sham-operated hamsters maintained under short
photoperiods, but not in the pinealectomized animals. The changes observed
in the Harderian glands and reproductive organs of hamsters kept in the short
photoperiod were not observed in the hamsters maintained in the long photoperiod. The photoperiod-induced ultrastructural changes in the hamster Harderian glands are most likely due to changes in hormonal levels brought about
by the regression of reproductive organs and can be prevented by pinealectomy.
In a n ultrastructural study of the hamster
Harderian gland, Bucana and Nadakavukaren (1972) identified a number of differences between the sexes, the major difference
being the presence of tubular clusters in the
male gland and the absence of these in the
female. Extensive dilated smooth endoplasmic reticulum, Golgi, and concentric lamellar formations are characteristics of the
female gland. Previous studies have also indicated that the sexual dimorphism of the
hamster Harderian gland is influenced by
steroid hormones andor gonadotropins. Castration of the male hamster resulted in the
gradual appearance of female characteristics
in the Harderian glands (Woolley and Worley, 1954; Hoffman, 1971; Clabough and Norvell, 1973; Payne et al., 1977; Lin and
Nadakavukaren, 1979). The development of
the female characteristics was prevented
when the castrated males were given daily
injections of testosterone propionate (Hoffman, 1971; Payne et al., 1977; Lin and Nadakavukaren, 1979) or blinded at the time of
castration (Hoffman, 1971; Clabough and
Norvell, 1973). The Harderian glands of
blinded female hamsters were shown to have
lowered levels of porphyrin and cellular char-
0 1984 ALAN R. LISS, INC.
acteristics which are normally found in the
male gland (Clabough and Norvell, 1974).
The conversion of the female Harderian
gland to a male type was prevented by pinealectomy a t the time of blinding (Clabough
and Norvell, 1974). Sun and Nadakavukaren
(1980) reported that the Harderian glands of
female hamsters developed male characteristics when the animals were treated daily
with testosterone propionate. Recently Nadakavukaren and Lin (1983) demonstrated
that the Harderian glands of male hamsters
exposed to short photoperiods developed female characteristics and vice versa. Data
presented in this paper demonstrate that pinealectomy can prevent the short-photoperiod-induced changes in the Harderian glands
of golden hamsters.
MATERIALS AND METHODS
Sexually mature male and female golden
hamsters (Mesocricetus auratus Waterhouse),
raised from a stock originally purchased from
Con Olson Company, Inc., Madison, WisconReceived August 8, 1983; accepted May 21, 1984.
Address reprint requests to M.J. Nadakavukaren, Biological
Sciences Department, Illinois State University, Normal IL 61761.
450
D.P. DIIORIA AND M.J. NADAKAVUKAREN
sin, USA, were maintained in either a short
photoperiod, 1:23 (lights on at 0800 hours, off
at 900 hours), or a long photoperiod 14:lO
(lights on a t 0800 hours, off at 2200 hours) a t
25°C. The groups of animals under the short
photoperiod were either pinealectomized or
sham-operated, while two similar groups
were maintained under the long photoperiod.
Each group consisting of 18 animals was housed separately with food and water given ad
libitum. Both pinealectomized and sham-operated male and female hamsters from each
photoperiod were killed by decapitation every
2 weeks, beginning a t 4 weeks after exposure
to experimental conditions and ending at 16
weeks. The Harderian glands were removed
and fixed for electron microscopy according
to Bucana and Nadakavukaren (1972).
Pinealectomy was performed by a combined method of Hoffman and Reiter (1965)
and Kuszak and Rodin (1976) while the hamsters were anesthetized with sodium pentobarbital (0.18 ml i.p./lOO-gm body weight).
Sham-operations were performed in the same
manner as pinealectomies except that the
pineal glands were not removed.
RESULTS
The Harderian glands of the sham-operated male hamsters maintained in the short
photoperiod showed cellular characteristics
that are typical of females (Fig. 1). Such
structures as membrane formations and dilated smooth endoplasmic reticulum appeared beginning with the 4-week samples.
During the same period clusters of membrane-bounded tubules were also found in
association with membrane formations. The
Harderian glands from the pinealectomized
males maintained in the short photoperiod
showed no significant changes from those of
the normal male hamsters (Fig. 2).
The Harderian glands of sham-operated female hamsters maintained in the short photoperiod
developed
male
cellular
characteristics (Fig. 3). This primarily included membrane-bounded clusters of tubules, while typical female characteristics
such as membrane formations and dilated
smooth endoplasmic reticulum gradually decreased. These changes first became apparent after 8 weeks of exposure to the short
photoperiod and continued until the end of
the experiment. The Harderian glands taken
from the pinealectomized females maintained in the short photoperiod showed no
significant change from those of normal female hamsters (Fig. 4).
Testicular and uterine sizes were greatly
reduced after 8 weeks in hamsters that were
sham-operated and exposed to the short photoperiod. This atrophy did not occur in animals that were pinealectomized.
Animals which were either sham-operated
or pinealectomized and then maintained in
the long photoperiod did not show any significant change in their Harderian glands during the 16 weeks of the experiment.
Testicular and uterine sizes remained normal in all animals that were exposed to the
14L:lOD photoperiod regardless of sham-operation or pinealectomy.
DISCUSSION
The data presented in this paper demonstrate that pinealectomy can prevent the
short photoperiod-induced ultrastructural
changes in the Harderian glands of male and
female hamsters. Our observations further
support the earlier suggestions that the Harderian gland is linked to the retinal-pinealgonadal axis (Wetterberg et al., 1970; Reiter
and Klein, 1971; Clabough and Norvell,
1973). It is of interest to note that the changes
in the Harderian gland ultrastructure also
corresponded to the time when the atrophy
of the reproductive organs occurred. Therefore, the ultrastructural changes may have
been induced by the altered hormone(s) levels accompanying testicular and uterine
atrophy. Earlier studies support this hypothesis in that the levels of testosterone, leutinizing hormone (LH) and follicle-stimulating
hormone (F'SH) decreased during short-photoperiod-induced testicular atrophy in male
Fig. 1. Acinar cell of sham-operated male hamster
after 12 weeks of exposure to 1L:23D photoperiod showing degeneration of tubular clusters (arrow) and formation of membrane whorls typical of females. ~37,000.
Fig. 2. Acinar cell of pinealectomized male hamster
after 12 weeks of exposure to 1L:23D photoperiod showing many tubular clusters (arrow) typical of normal
males. x40,OOO.
Fig. 3. Acinar cell of sham-operated female hamster
after 16 weeks of exposure to 1L.23D photoperiod showing tubular clusters which are typical of males (arrow).
X 37,000.
Fig. 4. Acinar cell of pinealectomized frmale hamster
after 16 weeks of exposure to 1L:23D photoperiod showing extensive smooth endoplasmic reticulum, Golgi (G),
and membrane formations (arrow) typical of normal females. x 37,000.
PINEALECTOMY, PHOTOPERIOD AND HARDERIAN GLAND
451
452
D.P. DIIORIA AND M.J. NADAKAVUKAREN
hamsters (Berndtson and Desjardins, 1974;
Tamarkin et al., 1976; Turck et al., 1976).
The hormonal patterns of the female hamsters with reduced uterine size induced by
short photoperiod also showed daily afternoon surges of LH and FSH (Seegal and
Goldman, 1975; Bridges and Goldman, 1975).
In addition, previous studies from our laboratory showed that testosterone has a significant role in regulating the sexual
dimorphism of the Harderian gland in the
golden hamster (Lin and Nadakavukaren,
1979; Sun and Nadakavukaren, 1980). Recent data further indicate that there are receptor sites for testosterone in the hamster
Harderian gland and that testosterone is metabolized by the gland (Hoh and Nadakavukaren, unpublished results). Therefore, there
is strong indirect evidence to suggest that
testosterone levels are more likely responsible for the observed ultrastructural changes
than the levels of LH and FSH.
ACKNOWLEDGMENTS
We thank Dr. John L. Frehn for the internal review of this paper.
LITERATURE CITED
Berndtson, W.E., and C. Desjardins (1974) Circulating
LH and FSH levels and testicular function in hamsters
during light deprivation and subsequent photoperiod
stimulation. Endocrinology, 95: 195-205.
Bridges, R.S., and B.D. Goldman (1975)Diurnal rhythms
in gonadotrophins and progesterone in lactating and
photoperiod induced acyclic hamsters. Biol. Reprod.,
13t617-622.
Bucana, C.D., and M.J. Nadakavukaren (1972) Fine
structure of the Hamster Harderian Gland. Z. Zellforsh., 129t178-187.
Clabough, J.W., and J.E. Norvell(1973) Effects of castration, blinding, and the pineal gland on the Harderian
glands of the male golden hamster. Neuroendocrinol-
ogy, 12:344-353.
Clabough, J.W., and J.E. Norvell(1974) Pineal influence
on the Harderian glands of female golden
hamsters.
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Hoffman, R.A. (1971) Influence of some endocrine glands,
hormones and blinding on the histology and porphyrins of the Harderian glands of golden hamsters. Am. J.
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Hoffman, R.A., and R.S. Reiter (1965) Pineal gland Influence on gonads of male hamsters. Science, 148:16091611.
Kuszak, J., and M. Rodin (1976) A new technique of
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short photoperiods on the ultrastructure of hamster
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Payne, A.P., J. McGadey, M.R. Moore, and G. Thompson
(1977) Androgenic control of the Harderian gland in
the male golden hamster. J. Endocrinol., 75t73-82.
Reiter, R.S., and D.C. Klein (1971) Observations on the
pineal gland, the Harderian glands, the retina, and
the reproductive organs of adult female rats exposed
to continuous light. J. Endocrinol., 51r117-125.
Seegal, R.F., and B.D. Goldman (1975) Effects of photoperiod on cyclicity and serum gonadotrophins in the
Syrian hamster. Biol. Reprod., 12223-231.
Sun, C.Y., and M.J. Nadakavukaren (1980) Effect of testosterone on the female hamster Harderian gland pigmentation and ultrastructure. Cell Tissue Res.,
207:511-517.
Tamarkin, L., S.S. Hutchinson, and B.D. Goldman (1976)
Regulation of serum gonadotrophins by photoperiod
and testicular hormones in the Syrian hamster. Endocrinology, 99: 1528-1533.
Turek, F.W., J.D. Alvis, J.A. Elliott, and M. Menaker
(1976) Temporal distribution of serum levels of LH and
FSH in adult male hamsters exposed to long or short
days. Biol. Reprod., 14t630-631.
Wetterberg, L., E. Geller, and A. Yuwiler (1970) Harderian gland An extraretinal photoreceptor influencing
the pineal gland in neonatal rats? Science, 167t884885.
Woolley, G.W., and J. Worley (1954) Sexual dimorphism
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ultrastructure, short, harderian, hamster, photoperiod, pinealectomy, induced, change, gland, prevention
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