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MICROSCOPY RESEARCH AND TECHNIQUE 34:133-138 (1996)
Sexual Dimorphism in the Harderian Gland of the Syrian
Hamster Is Controlled and Maintained by Hormones,
Despite Seasonal Fluctuations in Hormone Levels:
Functional Implications
GERALD R. BUZZELL
Department of Anatomy and Cell Biology, University of Alberta, Edmonton, Alberta T6G 2H7,Canada
KEY WORDS
Sexual dimorphism, Harderian gland, Syrian hamster, Histology, Porphyrin,
Lipid droplets, Photoperiods
ABSTRACT
The Harderian gland of the Syrian hamster (Mesocricetus aurutus) is unusual
amongst rodents in the degree of dimorphism present. Other types of hamsters have Harderian
glands which are apparently identical in male and female animals. Laboratory populations of
Syrian hamsters are derived from very limited genetic stock, which makes one concerned lest they
not be representative of wild populations; however, until wild stocks of M.uuratus become available, we should assume that insights derived from studies of dimorphism in Syrian hamsters
represent important considerations for the life of these animals. Two dimorphic features are the
histology and the porphyrin content of the Harderian glands. About 95% of the lipid droplets in
female glands are small (type l),whereas only about 65%of those in males is type 1,with the other
35% being type 2 (large droplets). Five weeks of castration of males led to an increase in type 1
droplets to 90%. On the other hand, 2 weeks treatment of females with testosterone led to a
reduction in type 1droplets to about 82%. Short day photoperiods led to a large increase in type 2
droplets in both males and females (to 52% in males, 35% in females after 8 weeks). These results
suggest that the lipid contained in type 2 droplets is important to hamsters of both sexes during the
winter. Porphyrin concentrations are 100-1,000 times higher in females than males, and this is
largely controlled by testosterone as orchidectomy leads to increased male levels and testosterone
treatment leads to reduced female levels. However, a number of treatments which also lead to
reduced testosterone levels do not lead to increased porphyrins and may, in fact, prevent the rise
which would normally follow orchidectomy. One of these antiporphyrinogenic treatments is exposure to short day photoperiods. Thus, the sexual differences in porphyrin levels in Syrian hamsters
are maintained, despite seasonal fluctuations in hormone levels. This suggests that this dimorphism is important for the fundion of the gland. o 1996 Wiley-Liss, Inc.
INTRODUCTION
It is now over 40 years since Christensen and Dam
(1953)and Wooley and Worley (1954) reported that the
Harderian glands of Syrian golden hamsters exhibit
marked sexual differences. Since that time, and particularly since the classic paper of Hoffman (19711,
Mesocricetus auratus has been a favourite experimental animal for researchers investigating Harderian
glands. We hope that understanding the hormonal control of dimorphic features will allow us to understand
the significance (i-e.,the function) of Harderian glands
in the overall biology of the hamster and that these
studies will contribute insights into problems with
wide biological importance.
SEXUAL DIMORPHISM IN SYRIAN HAMSTER
HARDERIAN GLANDS
The Extent of the Phenomenon
A list of characteristics known to differ between the
sexes in Syrian hamsters is given in Table 1. It is evi-
0 1996 WILEY-LISS, INC.
dent from this list that male and female Harderian
glands are quite different in Syrian hamsters.
However, Harderian glands are not the only features
of Syrian hamsters which differ in males and females.
For instance, females have high levels of a serum protein, called “female protein” (homologous to human
C-reactive protein and serum amyloid P component)
which is present in only very low concentrations in
males (Coe, 1977). Like dimorphism in the Harderian
gland, the significance of serum female protein is unknown.
Is the Syrian Hamster Harderian Gland Unique?
I have recently had the opportunity to examine
Harderian glands of several species of hamsters histologically. Male-female differences, if they exist a t all,
Received January 1, 1995; accepted in revised form March 16, 1996.
Address reprint requeste to Gerald R. Buzzell, Department of Anatomy and
Cell Biology, Universib of Alberta, Edmonton, Alberta T6G 2H7,Canada.
134
G.R. BUZZEU
TABLE I . Semially dimorphic features of Syrian (golden) hamster Harderian glands
Details
Reference
Feature
d
Larger
in
Size._.
_
Darkin P
Color
Hoffman, 1971
6:type I & II cells
Histology
4: type I cells
Bucana and Nadakavukaren, 1972
6:polytubular complexes
Ultrastructure
4: membranous organelles
Murawski et al., 1991
6: 3 types of alkyl-diacylglycerol
Lipids
Q : 2 types of alkyl-diacylglycerol
Lin and Nadakavukaren, 1981
6 : shorter chains
Fatty acids
Buzzell et al., 1991
Extra bands in 6 on SDS-PAGE
Proteins
Puig-Doming0 et al., 1988
4:more than d
Somatostatin
Hoffman, 1971
4:100-1,OOO times more than d
Porphyrins
Thompson et al., 1984
Mostly higher activity in P
Enzymes of porphyrin synthesis
Hoffman et al., 1985
Higher in P
Melatonin
Menendez-Pelaezet al., 1988
NAT higher activity in c3
Enzymes of melatonin synthesis
HIOMT higher activity in P
Hoffman and Jones, 1981
4:higher Na, Mn, Ca
Metals
6:higher Fe, Mo
McBlain et al., 1994
Higher,,B
in intact P
Androgen receptor
Payne et al., 1982
4:35 times more than S
Mast cells
Pangerl et al., 1989
More in P
B-receDtors
are not obvious in Djungarian (Phodopus sungorus),
Armenian (Cricetulus migrutorius), or Chinese (C. gresius) hamsters. It may or may not be significant that
Armenian hamsters also show smaller sex differences
in serum female protein levels than do Syrian hamsters (Coe and Ross, 1990).
This brings up an important question: Is Mesocricetus uurutus unique, and, if so, can we learn any general
truths from its study?
brandti) which we examined recently also showed gender differences.
These doubts notwithstanding, applying Occam’s razor to this problem dictates that we take what we see at
face value and assume that the dimorphism we see in
the laboratory evolved in the wild. Let us, therefore,
look at the control of some of these dimorphic features
in more depth. I will discuss the histology and the porphyrin content.
The Syrian Hamster
The Syrian hamster was first described by the brothers Alexander and Patrick Russell in 1797,from their
observations in Aleppo, a city in northern Syria (then
part of the Ottoman Empire). It was recognized as a
separate species and named by George Waterhouse, curator of the Zoological Society of London, in 1839.
The Syrian hamsters we u0e today are descendants of
three surviving hamster siblings, captured near
Aleppo by the zoologist Israel Aharoni of the Hebrew
University of Jerusalem in 1930.From these three animals are descended all of the hamsters in laboratories
and pet stores today. “here have been only two more
recent captures of wild Syrian hamsters, but I do not
believe that these are represented in the genotypes of
generally available hamsters (Murphy, 1985).
HARDERIAN GLAND HISTOLOGY
The Harderian glands are tubular glands, consisting
of secretory units with lipid-secreting cells arranged
around a central lumen. Nuclei are generally spherical
and basally located. Cytoplasm is often scanty, as most
of the cell is occupied by secretory lipid droplets.
Female Harderian glands contain cells whose lipid
droplets are typically small. It has been the practice in
the past to refer to these as type I cells (e.g., Hoffman,
1971). Ldpez et al. (19931,however, recently pointed
out that these cells differ ultrastructurally from type I
cells of male hamsters; they used the more noncommittal term “female secretory cell” to describe them. Most
of the secretory cells in the female gland are of this
type.
In male glands, cells whose light-microscopical appearance is identical to those of females are abundant.
These are the type I cells. In addition, another type of
cell has large secretory lipid droplets and generally
more abundant cytoplasm. These are type I1 cells.
We have looked in more detail at the secretory lipid
droplets in hamster Harderian glands by a morphometric approach. We considered small lipid droplets to be
type 1 and large lipid droplets to be type 2. We then
examined histologic sections under an ocular graticule
and counted (in several fields) the numbers of times the
graticule lines intersected over type 1 and type 2 droplets. From these numbers, we calculated the proportion
of each lipid droplet type in the section and, by extension, in the gland.
Is the Syrian Hamster in Captivity Similar to
That in the Wild?
Thus, despite its popularity in laboratories and pet
stores, all the Syrian hamsters we use are descended
from a very small gene pool. Thus, it is possible that
the sexual differences we see are due to a founder effect
which has bred true.
I fear that this doubt will be with us until wild hamsters from the Aleppo region are sampled and compared with captive populations, and I am enough of
a realist to doubt that this will happen soon. However, it may be relevant that Harderian glands from
the closely related Turkish hamsters (Mesocricetus
DIMORPHISM IN HAMSTER HARDERIAN GLAND
1 .o
Z
0
F
11L
0
1 .o
135
z
Z
0
-
k0.5
[L
0
11L
rx
0
a
0.5
0
DL
a
a
0.0
0.0
-
9
0
9
TES
LD
SD
Fig. 1. Effects of castration or short day photoperiods on proportions of type 1(clear bars) and type 2 (cross-hatched bars) lipid droplets in the Harderian glands of male Syrian hamsters. LD, long days
(14:lO);SD, short days (8:16).
Fig. 2. Effects of testosterone or short day photoperiods on proportions of type 1(clear bars) and type 2 (cross-hatched bars) lipid droplets in the Harderian glands of female Syrian hamsters. LD, long days
(14:lO);SD, short days (8:16);TES, given testosterone pellets.
The dimorphism in lipid droplets is thus apparent
quantitatively. Male glands typically have about 65%
type 1 lipid droplets, whereas those of females have
about 95% type 1droplets.
Androgen is a major control of this. Thus, castration
of male hamsters leads to an increase in type 1droplets
to 90% after 5 weeks (Fig. 1).On the other hand, beeswax pellets containing testosterone implanted into females for 2 weeks led to a significant reduction in type
1droplets to about 82% (Fig. 2).
These observations, while important, are based on
experimental procedures which do not occur in nature.
Androgen levels and levels of other hormones do, however, fluctuate naturally in hamsters, mediated by naturally occurring decreased day length in the autumn.
This is the basis of seasonal reproduction. Syrian hamsters interpret less than 12.5 h of light per day as a
short day; serum gonadotrophin, prolactin, thyroid hormone, and sex steroid levels decrease. In males, the
testes and accessory sex glands atrophy due to low testosterone levels. Females become anestrous, their ovaries hypertrophy, and their uteri atrophy. These
changes reverse spontaneously in the spring. The phenomenon of seasonal reproduction is controlled by the
pineal gland, as pinealectomy prevents these changes
from occurring (Reiter, 1981).
Exposure of male hamsters to short days reduces testosterone levels; however, it does not mimic castration.
In fact, the opposite is true. Type I1 cells predominate
and morphometric studies confirm that type 1 lipid
droplets decreased from 64% in long days to 48% in
short days (Fig. 1).
Female hamsters react to short days in a similar
manner to males. Eight weeks in short days lead to a
conspicuous increase in type I1 cells. The percentage of
type 1 lipid droplets decreased from 94% to 65% (Fig.
2).
To summarize, Harderian lipid droplets in both
males and females change their characteristics with
the approach of winter, suggesting a function in adaptation to cold weather. This change may be, for instance, in the viscosity of the lipid and suggests that
the theory of Thiessen (1992) that Harderian secretions
are groomed into the pelage in winter to insulate the
animal may be correct. We are studying Harderian lipids in relation to the photoperiod to try to clarify this
matter.
PORPHYRIN IN HARDERIAN GLANDS
High porphyrin concentrations are a feature of most
rodent Harderian glands, and the significance of this is
unknown. The sex difference in Harderian porphyrin
concentrations in Syrian hamsters is truly remarkable.
In our experience, male porphyrin levels are in the
4-10 ng/mg tissue range, whereas those of females are
in the 1-4 pg/mg range. In other words, female Harderian glands have 100-1,000 times higher porphyrin
levels than those of males. This is reflected in the external appearance of the glands (male glands are pale;
those of females are dark) and in histology, as female
glands show deposits of precipitated porphyrin.
Thus, dimorphism is seen by a huge preponderance
of porphyrins in female glands over those of males.
This is largely controlled by androgens. Thus, castrating males leads to a very rapid and very striking rise in
porphyrin concentrations. Within 1 week, there is a
tenfold rise in porphyrin concentrations, and within
4-6 weeks porphyrin concentrations near those of fe-
G.R. BUZZELL
L
0
1
2
3
WEEKS CASTRATED
Fig. 3. Effects of castration of up to 3 weeks duration on porphyrin
concentrations in the Harderian glands of male Syrian hamsters.
Data from Buzzell et al. (1991).
males are achieved (Fig. 3) (Buzzell et al., 1991). On
the other hand, treating a female hamster with testosterone leads to a decrease in porphyrin concentrations
(though not so precipitous nor so striking as the rise
seen in males) (Buzzell et al., 1992).
Thus, low testosterone levels lead to high porphyrin
levels, whereas high testosterone levels have the opposite effect. However, not all procedures which lower
testosterone levels lead to elevated porphyrin concentrations, and these procedures may prevent most of the
porphyrinogenesis resulting from castration. Procedures with this antiporphyrinogenic effect include hypophysectomy, blinding, and short day photoperiods
(Fig. 4) (Buzzell et al., 1994; Hoffman, 1971; Hoffman
et al., 1990).
These observations suggested that some hormone
whose levels are altered by short photoperiod (but not
by castration) is necessary for low testosterone levels to
induce porphyrinogenesis. Prolactin is such a hormone.
Prolactin secretion is unusual amongst pituitary
hormones in that its release is chronically inhibited by
hormones of the hypothalamus. Dopamine is the major
prolactin release inhibiting hormone. Bromocriptine is
an ergot alkyloid which is a dopamine agonist; it is
used experimentally and clinically to suppress prolactin secretion. We therefore treated hamsters with bromocriptine to determine whether lowering prolactin
levels also prevents the porphyrinogenic effects of castration.
We found our hypothesis confirmed. Bromocriptine
had no effect on Harderian porphyrin levels in intact
males. In castrated males, however, bromocriptine prevented most of the rise which follows castration in its
absence (Buzzell et al., 1989).
Further experiments strengthened this relationship.
Removal of the pituitary had a similar effect to short
days or bromocriptine: no significant rise in porphyrins, whatever the gonadal state. However, removal of
the pituitary and its replacement in the sella turcica or
its insertion under the kidney capsule, procedures
-
-
LD
LO
SD
SD
INTACT
CAS
INTACT
CAS
Fig.4. Effects of castration and photoperiod on porphyrin concentrations in the Harderian glands of male Syrian hamsters.CAS,castrated; LD,long days (1410);SD, short days (816).Data from Buzzell
et al. (1994).
which restore prolactin secretion while keeping levels
of other pituitary hormones low, led to full or partial
restoration of Harderian porphyrin levels to those seen
after castration (Fig. 5) (Buzzell et al., 1992).
Thus, the evidence is good that the control of Harderian porphyrins in male hamsters involves the interaction of at least two hormones: testosterone and prolactin. In addition, we have evidence that thyroid
hormones are also involved but in a way which we have
not yet sorted out. Both hypothyroid and hyperthyroid
conditions prevent the porphyrinogenic effects of castration (Hoffman et al., 1989, 1990).
Female porphyrin levels are high and are difficult to
alter experimentally. Testosterone treatment, hypophysectomy, hypothyroidism, or hyperthyroidism
leads to a drop in female hamster porphyrin levels
(Buzzell et al., 1992; Hoffman et al., 1989, 1990; Marrufo et al., 1989). However, none of these treatments
leads to levels as low as those of males. Other endocrine
paradigms, some of which prevent the rise in porphyrin
levels following castration in males (e.g., short days,
bromocriptine), have no effect on female porphyrin levels (Buzzell et al., 1989, 1994; Hoffman et al., 1990;
Menendez-Pelaez et al., 1992; Rodriguez-Colunga et
al., 1991; Spike et al., 1985, 1990).
FUNCTIONAL IMPLICATIONS
The Harderian gland of Mesocricetus uurutus is unusual in the degree of sexual dimorphism displayed.
Striking amongst dimorphic features are porphyrin
content and lipid droplet types. Both are under androgenic control; however, they respond to seasonal fluctuations in androgen levels in different ways.
Porphyrin levels are kept low in males and high in
females, despite seasonal fluctuations in reproductive
DIMORPHISM IN HAMSTER HARDERIAN GLAND
0.0 J
1
137
A., Pangerl, B., Vaughan, M.K., and Reiter, R.J. (1989) Bromocriptine prevents the castration-induced rise in porphyrin concentration in the Harderian glands of the male Syrian hamster, Mesocricetus auratus. J. Exp. Zool., 249:172-176.
Buzzell, G.R., Menendez-Pelaez,A., Chlumecky, V., and Reiter, R.J.
(1991) Gender differences and time course of castration-induced
changes in porphyrins, indoles, and proteins in the Harderian
glands of the Syrian hamster. Can. J. Physiol. Pharmacol., 69:
1814-1818.
Buzzell, G.R., Hoffman, R.A., Vaughan, M.K., and Reiter, R.J. (1992)
Hypophysectomy prevents the castration-induced increase in porphyrin concentrations in the Harderian glands of the male golden
hamster: A possible role for prolactin. J. Endocrinol., 133:29-35.
Buzzell, G.R., Menendez-Pelaez,A., Hoffman, R.A., Rodriguez, C., and
Antolin, 1. (1994) The androgenic control of porphyrin in the Harderian glands of the male Syrian hamster is modulated by the photoperiod, which suggests that the sexual differences in porphyrin
concentrations in this gland are important functionally. Anat. Rec.,
24052-58.
v
L
HPX
rAP1
L
A
Fig. 5. Effects of hypophysectomy (HPX) and removal of the anterior pituitary and its reinsertion into the sella turcica ([API) on
porphyrin concentrations in the Harderian glands of castrated male
Syrian hamsters. Data from Buzzell et al. (1992).
hormone levels. We do not yet know what the function
of this porphyrin is. However, the fact that nature has
designed a complex homeostatic control system implies
that the marked sexual differences in the concentrations of Harderian porphyrin are critical to the functions of both the Harderian glands and their porphyrin
in this species.
Lipid droplet types, while also being controlled by
androgens, are not consistent year round. Thus, both
male and female glands have increased amounts of
type 2 lipid in the short days of autumn and winter,
suggesting that this feature is important to the animal
at this time of the year.
Again, we do not know the function of either Harderian porphyrin or lipid. Nor do we know how universally applicable these results are. However, I feel that
knowledge of the Harderian gland in one species is an
important step towards a more general understanding.
I hope that this is a contribution toward that goal.
ACKNOWLEDGMENTS
I am especially indebted to Roger Hoffman and Russel Reiter, my friends and collaborators. Studies in my
laboratory are funded by the Canadian Natural Sciences and Engineering Research Council.
Several of the studies described here were done in
collaboration with the late Armando Menhdez-Pellez.
His recent death was a shock t o all of us. The field of
Harderian gland research has lost a major player; I
have lost a good friend and colleague.
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