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Original Studies |
and ß in the Human Reproductive Organs
Oncology and Molecular Endocrinology Research Center, Laval University Hospital (CHUL), and Laval University, Québec, Canada G1V 4G2
Address all correspondence and requests for reprints to: Dr. Georges Pelletier, Oncology and Molecular Endocrinology Research Center, Laval University Hospital (CHUL), 2705 Laurier boulevard, Québec, Québec, Canada G1V 4G2. E-mail: georges.pelletier{at}crchul.ulaval.ca
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Abstract |
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 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
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and the recently discovered ERß, in
human reproductive tissues. In the ovary, ERß immunoreactivity was
found in nuclei of granulosa cells of growing follicles at all stages
from primary to mature follicles, interstitial gland, and germinal
epithelium cells. Nuclear staining for ER occurred in thecal,
interstitial gland, and germinal epithelium cells. In the uterus,
strong ER immunoreactivity was detected in nuclei of epithelial,
stromal, and muscle cells. Similar localization was obtained for ERß,
although the staining was much weaker. In the vagina, only ER could
be detected; a nuclear reaction was observed in deep layers of the
stratified epithelium as well as in stromal and muscle cells. In the
mammary gland, both ER subtypes were observed in epithelial and stromal
cells. In the testis, ERß was detected in nuclei of Sertoli and
Leydig cells, whereas ER immunoreactivity was only observed in
Leydig cells, with no tubular labeling. In the efferent ducts, only
ERß could be detected, whereas neither ERß nor ER could be found
in the epididymis. In the prostate, ERß nuclear immunolabeling was
observed in both basal and secretory cells in alveoli as well as in
stromal cells, whereas ER could not be detected. The present results
demonstrate that there is a cell-specific localization for each of the
ER subtypes in the majority of the reproductive organs studied.
Moreover, they contribute to establish the exact sites of action of
estrogens in male and female human reproductive systems. |
Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Recently, a second ER, called ERß, has been cloned from the rat
prostate (8) and the original ER is now designated the
ER subtype. The ERß protein is highly homologous to ER. It
shares with the ER protein about 95% homology in the DNA-binding
domain and 60% homology in the ligand-binding domain. The mouse and
human ERß have also been cloned and shown to have similar
relationships to ER (9, 10). During the last few years,
the development of specific molecular probes to detect each ER subtype
messenger ribonucleic acid (mRNA) and of specific antibodies to ER
and ERß has allowed studies of the distribution of the ER subtypes.
Most of the studies of ER subtype expression to date have been
performed in the rat (11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21).
In the rat prostate, ERß was localized to the secretory epithelial
cells, in contrast with an absence or a very low expression of ER
(19, 21). In the testis, ERß was detected in the nuclei
of Sertoli and germ cells, whereas ER immunoreactivity was observed
in Leydig cells and was also associated with germ cells (16, 19). In seminal vesicles, ERß was localized to nuclei of
epithelial and stromal cells, whereas ER was only poorly expressed
in the same cell types (15, 19). In ovaries, ERß was
detected in granulosa cells of growing follicles, whereas ER was
poorly expressed, being located in theca interna and interstitial cells
(11, 13, 14, 19). In the uterus, the reverse situation was
found, with high expression of ER in epithelial, stromal, and muscle
cells and very low expression of ERß (11, 14, 15, 19).
To date, there have been few studies on the localization of ER and
ERß in human and monkey tissues (22, 23, 24, 25).
More information about the physiological roles of the two ER subtypes
in reproduction has been obtained from mice lacking ER or ERß
(26, 27). Male and female animals deficient in ER
appeared to be infertile. In mice lacking ERß, both males and females
were fertile, although reduced ovarian efficiency was observed. These
findings suggest that each of the ER subtypes plays a distinct
physiological role in reproduction. To clarify the involvement of ER
and ERß in human reproduction, it appeared of interest to identify
the cell types expressing the two ER subtypes in human reproductive
tissues, including the mammary gland. In the present study we used
specific antibodies to localize ER and ERß proteins by
immunocytochemistry.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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This study was approved by the institutional review board at
Laval University Medical Center. All of the patients signed informed
consent forms before participation in this research project. The
samples of reproductive tissues, i.e. testis, prostate,
ovary, uterus, and breast, were all obtained at surgery. The specimens
used in the present immunocytochemical studies had a volume of about
2.5 cm3, with the exception of prostate
chippings, which were smaller (
0.4 cm3). They
were fixed in 4% paraformaldehyde in 0.2 M
phosphate buffer (pH 7.4) within 15 min after they had been dissected
out. The average fixation time was 12 h. The tissues were then
dehydrated through increasing concentrations of ethanol, cleared in
toluene, and embedded in paraffin. Ovaries, uterus, and breast tissues
were obtained from premenopausal patients (25–40 yr of age). Prostate
tissue was obtained from patients with symptomatic benign prostatic
hyperplasia undergoing transurethral prostatectomy. The age of male
patients ranged from 55–70 yr. In each case, a minimum of three
separate tissues was studied, and the results were consistent.
Immunocytochemistry
Paraffin sections (5 µm) were deparaffinized, hydrated, and
then treated with 3% H2O2
in PBS (pH 7.6) for 30 min. These steps were followed by heating the
sections in a microwave oven for antigen retrieval using citrate buffer
(pH 5.5) as previously described (28). The sections were
then incubated overnight at 4 C with ER antibody (see below for
details) at a concentration of 1 µg/mL or with ERß antibody (2
µg/mL; see below for details). Control sections were incubated with
preadsorbed antibodies as described below. Sections were then washed in
Tris-saline (pH 7.6) and incubated at room temperature for 4 h
with peroxidase-labeled goat antirabbit 
-globulin (HyClone Laboratories, Inc., Logan, UT) diluted at 1:500 as previously
described (29).
ER. To localize ER we used an affinity-purified rabbit
polyclonal antibody (HC-20, Santa Cruz Biotechnology, Inc., Santa Cruz, CA) raised against a synthetic peptide
corresponding to amino acids 580–599 mapping at the carboxyl-terminus
of the ER of human origin. This antibody reacts specifically with
the human ER2 by Western blotting,
immunoprecipitation, and immunocytochemistry. It was used at a
concentration of 1 µg/mL. For control experiments, the antibody was
adsorbed by preincubation with 20 µg peptide for 2 h at room
temperature.
ERß. For ERß localization, we used a rabbit polyclonal
antibody (06–629, Upstate Biotechnology, Inc., Lake
Placid, NY) directed against a synthetic peptide corresponding to amino
acids 46–63 of human ERß. By Western blotting, it recognizes ERß
of approximately 65 kDa, but does not detect ER. The antibody was
used at a concentration of 2 µg/mL. For a specific control, the
antibody was adsorbed by preincubation with 20 µg peptide for 2
h at room temperature.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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In the ovary, immunocytochemical studies conducted with the
specific antibody to ERß revealed that nuclear staining occurred in
granulosa cells of the growing follicle at all stages from primary to
mature follicles (Fig. 1
). Scattered
interstitial gland cells and germinal epithelium cells also exhibited
nuclear staining. The primordial follicles and corpora lutea were
unlabeled. ER immunoreactivity was detected in nuclei of theca
interna cells, interstitial gland cells, and germinal epithelium cells
(Fig. 2). Granulosa and
corpora lutea cells did not exhibit any staining.
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produced a strong nuclear
reaction in both luminal and glandular epithelial cells (Fig. 3
). In
the stroma, in which glands are embedded, labeled cells were also
observed. Nuclear staining was consistently found in muscle cells.
Using antibodies to ERß, weak staining was observed in nuclei of the
epithelial cells. In the stroma and muscle, only a very few cells
appeared to be weakly labeled. In the vagina, ER nuclear staining
was observed in the deep layers of the stratified epithelium as well as
in the cells of the lamina propria and smooth muscle cells (Fig. 4). No
ERß immunoreactivity could be detected.
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immunoreactivity was present in the
nuclei and to a lesser degree in the cytoplasm of epithelial cells of
intralobular acini and interlobular ducts. A few stromal cells also
exhibited nuclear labeling. Similar cellular localization was observed
after immunostaining with ER-ß antibodies. In the latter case,
cytoplasmic staining was more prominent than that observed with
anti-ER (Fig. 5). Male reproductive organs
In the testis, ER was only detected in the nuclei of Leydig
cells; the tubules were totally devoid of any reaction. ERß
immunostaining was found in nuclei of cells located at the periphery of
the tubules, which are probably Sertoli cells, and also in Leydig cells
(Fig. 6). Nuclear immunostaining for ERß, but not for ER, was
found in the epithelial cells in the rete testis and efferent ducts
(Fig. 7). Neither ER nor ERß could be detected in the ducts of the
epididymis.
In the prostate, only ERß immunoreactivity could be demonstrated.
Staining was generally localized in nuclei of all the basal cells and
the vast majority of secretory cells in alveoli. Several stromal cells
exhibiting nuclear labeling were consistently observed (Fig. 8).
In all of the reproductive organs studied as well as in mammary glands,
immunolabeling was completely abolished by immunoadsorption of the
antibody with the corresponding antigen (Figs. 1 and 3). The
differential cellular localization of each receptor subtype in the
majority of the tissues studied is also highly indicative of the
specificity of the antibodies used to detect the ER subtypes.
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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and ERß, we demonstrated the
histological localization of the two ER subtypes in human reproductive
organs. To date, most of the localization studies have been performed
in rodents (11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21). In fact, the only histological data
on the expression of ERs in adult human tissues were obtained by
in situ hybridization (22). In the ovary, ERß
was expressed in granulosa cells of growing follicles at all stages,
with the exception of primordial follicles, and also in some
interstitial gland cells. These findings agree with previous reports
showing high levels of ERß mRNA in granulosa cells of human
(22) and monkey (25) follicles. By
immunocytochemistry, the ERß protein has been localized in granulosa
cells of growing follicles in the rat (13, 14, 19).
Immunoreactive ER was detected in thecal and interstitial gland
cells, confirming previous observations in the rat ovary (13, 19). The ERß is probably involved in the influence of
estrogens in the growth and development of ovarian follicles. In fact,
estrogens have been shown to stimulate the proliferation of granulosa
cells in small follicles, increase granulosa cell gonadotropin receptor
levels, and modulate progesterone production by the granulosa cells
(30, 31). Moreover, disruption of the ER gene could not
eliminate the ability of small follicles to grow, as shown by the
presence of secondary and antral follicles in ER knockout mice
(26). It is conceivable that estrogen’s effect on
follicular and thecal cells might be mediated by ERß and ER,
respectively. Although both receptor subtypes might be involved in
interstitial gland cell function, the precise role and mechanism of
action of estrogens in the human ovary remain to be elucidated. Studies
in female mice lacking aromatase, ER, or ERß indicate that the two
known ERs are required for normal ovarian function (26, 27, 32).
A finding that might be of interest is the localization of both
receptor subtypes in the germinal epithelium of the ovarian surface.
ER and ERß have also been found in the germinal epithelium in rat
(13, 19) and monkey (25) ovary, respectively.
Most human ovarian cancers originate from the germinal epithelium
(33). Recently, Brandenberger et al.
(34) reported a decrease in ERß expression in carcinomas
of the human ovary. The relationship between ER expression and the
development of human ovarian cancer remains to be further
investigated.
In the uterus, intense nuclear ER staining occurred in the luminal
and glandular epithelial cells, stromal cells, and muscle cells. In
contrast, we observed only weak ERß staining. These results agree
well with data indicating that in the human uterus, the expression of
ER mRNA was predominant (22). In the monkey, ERß mRNA
has been detected by in situ hybridization in epithelial,
stromal, and muscle cells (25). In rat uterus, it has been
found by immunocytochemistry that ER, but not ERß, was expressed
in epithelial, stromal, and muscle cells (13, 19, 35). In
mutant mice without functional ERß, the development of uterus and
oviducts appeared normal (27). These deficient mice,
although they had reduced fertility, had normal pregnancy and delivery.
These results then suggest that, at least in the female mouse, ERß is
not essential for normal functions of the reproductive tract. It is
then likely that ER is the ER subtype involved in the mediation of
the major effects of estrogen in the uterus. Mice deficient in ER
are infertile and exhibit atrophy of oviduct and uterus
(26).
In the mammary gland, both ER subtypes were found in the epithelial
cells of alveoli and ducts as well as in stromal cells. The present
data are in agreement with previous results indicating the presence of
the classical ER (probably ER) in both epithelial and stromal cells
in human mammary tissue (36). Our results also agree well
with recent findings indicating that both ER and ERß mRNA are
expressed in human breast as well as in breast tumors
(22). Moreover, several human breast epithelial cells have
been shown to be both ER and ERß positive (37). The
respective roles of the ER subtypes in physiology of the mammary gland
and the development of breast cancer remain to be clarified.
In the testis, ER immunoreactivity was observed in nuclei of Leydig
cells, whereas ERß staining could be detected in nuclei of both
Sertoli and Leydig cells. Using in situ hybridization,
Enmark et al. (22) observed that in human
testis ERß mRNA was detected in the seminiferous epithelium with no
labeling of Sertoli cells. The discrepancy between the present results
describing ER proteins and those obtained by in situ
hybridization (22) remains to be fully clarified. The
presence of ERß in Sertoli cells suggests that estrogens might
influence germ cell function and maturation. The presence of ER and
ERß in nuclei of Leydig cells confirms previous results obtained in
the rat (16, 19). Both ER subtypes might be involved in
the local feedback regulation of steroidogenesis and/or Leydig cell
differentiation. The presence of ERß, and not ER, in efferent
ducts and the absence of ERs in epididymis differs from previous
reports indicating that in rodent epididymis, both ER subtypes are
expressed (8, 11, 16).
In a man with estrogen resistance caused by a mutation of ER,
clinical examination revealed that he had normal sized testis and
prostate (38). Serum testosterone and sperm density were
also within the normal range. This suggests that in humans, ER is
not essential for normal testicular function. This is concordant with
the present findings and the previous observation that ERß mRNA
expression is predominant (22) in man. In contrast, adult
male mice lacking functional ER exhibit reduced testicular size and
are infertile, whereas male mice deficient in ERß can reproduce
normally (26, 27).
In the prostate, ERß was expressed in both basal and secretory cells
in alveoli as well as in stromal cells, whereas no ER could be
detected. This is in agreement with findings obtained in the rat
prostate indicating that ERß was the predominant ER subtype (8, 11, 19). Enmark et al. (22) reported
higher levels of ERß mRNA than ER mRNA in human prostate cancer.
Using in situ hybridization, we showed that in monkey
prostate, ERß mRNA was detected in epithelial cells
(25). The role of estrogens in prostate development and
function is still unknown. It has been recently shown that ERß
knockout mice develop prostate hyperplasia (27). This
suggests that ERß may be involved in negative regulation of prostatic
cell proliferation.
In summary, the present data clearly demonstrate a cell-specific
localization for each of the ER subtypes in human reproductive organs.
In the ovary, each receptor subtype could exert different functions
according to their specific cellular localization. In the uterus and
vagina, ER is most likely the subtype involved in estrogen’s
effects. The differential localization of ER and ERß in the testis
and prostate is indicative that both ER subtypes might be involved in
the influence of estrogens on male reproductive function.
Received April 11, 2000.
Revised July 10, 2000.
Revised August 10, 2000.
Accepted August 24, 2000.
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I. Stavrou, C. Zois, J.P.A. Ioannidis, and A. Tsatsoulis Association of polymorphisms of the oestrogen receptor{alpha} gene with the age of menarche Hum. Reprod., April 1, 2002; 17(4): 1101 - 1105. [Abstract] [Full Text] [PDF]
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 L. O'Donnell, K. M. Robertson, M. E. Jones, and E. R. Simpson Estrogen and Spermatogenesis Endocr. Rev., June 1, 2001; 22(3): 289 - 318. [Abstract] [Full Text] [PDF]
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S. F. Palter, A. B. Tavares, A. Hourvitz, J. D. Veldhuis, and E. Y. Adashi Are Estrogens of Import to Primate/Human Ovarian Folliculogenesis? Endocr. Rev., June 1, 2001; 22(3): 389 - 424. [Abstract] [Full Text] [PDF]
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S. Makinen, S. Makela, Z. Weihua, M. Warner, B. Rosenlund, S. Salmi, O. Hovatta, and J.-A. Gustafsson Localization of oestrogen receptors alpha and beta in human testis Mol. Hum. Reprod., June 1, 2001; 7(6): 497 - 503. [Abstract] [Full Text] [PDF]
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 J. Teng, Z.-Y. Wang, and D. E. Bjorling Estrogen-induced proliferation of urothelial cells is modulated by nerve growth factor Am J Physiol Renal Physiol, June 1, 2002; 282(6): F1075 - F1083. [Abstract] [Full Text] [PDF]
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