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Departments of Urology (G.S.P., M.M., C.W., W.C., L.B.) and Physiology and Biophysics (G.S.P.), University of Illinois College of Medicine, Chicago, Illinois, 60612; and Center for Biotechnology and Department of Medical Nutrition, Karolinska Institute (G.K., J.-Å.G.), Huddinge, Sweden
Address all correspondence and requests for reprints to: Gail S. Prins, Ph.D., Department of Urology, M/C 958, 820 South Wood Street, Chicago, Illinois 60612. E-mail: gprins{at}uic.edu
Neonatal exposure to estrogens permanently alters rat prostate growth
and epithelial differentiation leading to prostatic dysplasia on aging.
The effects are lobe-specific, with the greatest response observed in
the ventral lobe. Recently, a novel estrogen receptor (ER)
complementary DNA was cloned from the rat prostate and termed ER-ß
(ERß) due to its high homology with the classical ER
. The protein
possesses high affinity for 17ß-estradiol, indicating that ERß is
an alternate molecule for mediating estrogenic effects. Importantly,
ERß messenger RNA (mRNA) was localized to rat prostatic epithelial
cells, which contrasts with the stromal localization of ER in the
rat prostate. The present study was undertaken to determine the
ontogeny of ERß mRNA expression in the rat prostate lobes and to
examine the effects of early estrogen exposure on prostatic ERß
expression. Male rat pups were given 25 µg estradiol or oil on days
1, 3, and 5; were killed on day 1, 3 (oils only), 6, 10, 30, or 90; and
prostate lobes were frozen. Longitudinal sections were processed for
in situ hybridization using an 35S-labeled
antisense mRNA probe corresponding to a 400-bp
EcoRI-AccI fragment in the 5'untranslated
region of rat ERß complementary DNA. Image analysis was used to
quantitate silver grains. In addition, total RNA was isolated from the
ventral prostate (VP) and used for semiquantitative RT-PCR. Results
from in situ hybridization revealed that at birth, ERß
was equivalently expressed at low levels in both mesenchymal and
epithelial cells in oil-treated rats. From day 1 onwards, expression in
all stromal cells slowly and significantly declined, so that in the
control adult prostate, stromal ERß mRNA was slightly above
background. In the oil-treated control rats, epithelial ERß mRNA
increased to moderate levels between days 6–10 in the VP and days
10–15 in the dorsal and lateral lobes as cells began differentiation
and ducts lumenized. A further significant increase in ERß message
was observed at day 30, which indicates that full epithelial ERß
expression may require the completion of functional differentiation. By
day 90, expression levels were maximal and similar between the lobes.
RT-PCR substantiated this developmental increase in ERß between days
1–90. Neonatal exposure to estrogens did not have an immediate effect
on prostatic ERß mRNA levels as determined by in situ
hybridization and RT-PCR. However, the marked increase in epithelial
cell expression at day 30 observed in the control VP was dampened in
the VP of animals exposed neonatally to estrogens. By day 90, the VP of
estrogenized rats possessed low ERß message levels compared with the
high expression in oil controls. In contrast, the dorsal and lateral
lobes of neonatally estrogenized rats possessed high levels of ERß
mRNA at day 90, equivalent to controls. The present data demonstrate
that ERß mRNA expression in the rat prostate is developmentally
regulated, and that neonatal estrogen can affect this expression in the
adult VP. Because the effect of neonatal estrogens was not immediate,
the data imply that early estrogen exposure may not directly
autoregulate ERß expression, and suggests that the adult effects on
ERß mRNA expression may be indirect. The differences in ERß mRNA
imprinting in the separate lobes may account for or reflect the
lobe-specific neonatal estrogen imprints previously observed in the rat
prostate.
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