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in Bovine Endometrial Cells1
Centre de Recherche en Reproduction Animale, Faculté de Médecine Vétérinaire, Université de Montréal, St-Hyacinthe, Québec J2S 7C6, Canada
Address all correspondence and requests for reprints to: A. K. Goff, Centre de Recherche en Reproduction Animale, Faculté de Médecine Vétérinaire, Université de Montréal, 3200 Rue Sicotte, St-Hyacinthe, Québec J2S 7C6, Canada. E-mail: goffak{at}medvet.umontreal.ca
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResultsDiscussionReferences |
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(IFN-) alters PG synthesis during early pregnancy in
ruminants. In this study, we examined the effects of these steroid
hormones and recombinant bovine IFN- (rbIFN-) on PG production
and on cyclooxygenase-2 (COX-2) and PG F (PGF) synthase (PGFS) gene
expression in isolated endometrial cells. E2 decreased both
PGF2
and PG E2 (PGE2) whereas
progesterone increased PGF2 secretion in epithelial
cells. Steroid hormones had no effect on PG production in stromal
cells. rbIFN- attenuated both PGF2 and
PGE2 production in epithelial cells and enhanced their
production, and the ratio of PGE2 to PGF2,
in stromal cells. Northern blot analysis showed that E2 and rbIFN-
decreased COX-2 messenger RNA (mRNA) levels in epithelial cells.
Conversely, rbIFN- increased COX-2 mRNA in stromal cells.
Furthermore, rbIFN- decreased PGFS mRNA in both cell types and this
was associated with the increase in
PGE2/PGF2 ratio. These results show that the
regulation of PG synthesis by steroid hormones is different in
endometrial epithelial and stromal cells in vitro. The
attenuation of PGF2 secretion from epithelial cells and
increased PGE2 production in stromal cells by rbIFN- are
modulated by steroid hormones. |
Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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(PGF2)
and PG E2 (PGE2) are major secretory products
of the uterine endometrium in ruminants (1). PGF2,
primarily secreted from the surface epithelium of the uterus, is the
luteolytic agent in livestock (2, 3, 4, 5). PGE2 protects the
corpus luteum (CL) from spontaneous regression (6) and may play a role
in pregnancy maintenance. In ovariectomized guinea-pig, rat, and sheep
(1), uterine PGF2 concentrations are low and are
restored to normal after treatment with progesterone (P4) followed by
estrogen. In cultured bovine uterine endometrial epithelial cells, but
not stromal cells, the basal production of PGF2 and
PGE2 was reduced by estradiol (E2) and increased by P4 (7).
The control of PGE2 secretion might differ from that of
PGF2, because PGE2 secretion from the
endometrium does not show the same cyclical changes as
PGF2 (1). Ovarian steroids play an important role in the
regulation of endometrial PG synthesis, but the sites and mechanisms of
action have not been determined (1).
Interferon- (IFN-) is produced by the trophoblast tissue, between
days 15–24 of gestation (8), and prevents luteolysis by suppressing
endometrial PGF2 secretion. Intrauterine infusion of
recombinant bovine IFN- (rbIFN-) prolonged the luteal lifespan in
cows (9). Administration of IFN- attenuated the episodic release of
uterine PGF2 by down-regulation of estrogen receptor and
oxytocin receptor expression (10). In vitro, natural bovine
IFN- significantly diminished basal PGF2 (but not
PGE2) secretion by bovine uterine endometrial explants (11, 12). rbIFN- significantly diminished both basal PGF2
and PGE2 secretion by bovine endometrial epithelial cells
(12, 13, 14, 15). Natural ovine IFN- diminished both basal
PGF2 and PGE2 secretion by ovine endometrial
epithelial cells (16).
Cyclooxygenase (COX) is the key rate-limiting enzyme responsible for
the conversion of arachidonic acid to PGG2 and
PGH2, the precursor for PGF2,
PGE2, and other members of PG family (17). Two isoforms of
COX (COX-1 and COX-2) have been identified in mammalian cells. COX-1 is
a constitutively expressed enzyme; COX-2 is highly induced by various
inducers, such as phorbol esters, mitogens, cytokines, and serum
(18, 19, 20). PG F synthase (PGFS) was first discovered in rabbit liver by
Wong (21). The purified PGFS from bovine lung catalyzed the reduction
of PGH2 to PGF2, PGD2 to a
stereoisomer of PGF2 (9, 11ß-PGF2)
(22). A PGFS transcript from bovine lung was about 1.4 kb (23).
However, the uterine endometrial expression and regulation of PGFS have
not been reported.
The regulation of COX-2 and PGFS expression by steroids and IFN- are
not well understood. Arslan and Zingg (20) found that both IL-1ß and
TNF induced PGF2 release and COX-2 messenger RNA
(mRNA) expression in rat uterine stromal cells in vitro. A
recent study in sheep (24) showed that COX-1 protein was expressed at
steady-state levels in the endometrium during the estrous cycle and
during comparable stages of pregnancy. In contrast, COX-2 protein was
highly and transiently expressed from days 12–15 of the estrous cycle
and declined, thereafter, to undetectable levels. Endometrium from
early pregnant ewes showed a similar pattern of COX-2 expression,
although there was a slower decrease beyond day 15. P4 induced
endometrial COX-2, and E2 slightly increased COX-2 expression, but only
after P4 priming (24).
rbIFN- has no significant effect on COX-1 mRNA expression (2.8 kb
mRNA) in bovine endometrial epithelial cells (14) and ovine endometrial
COX-1 mRNA is not regulated by the conceptus (17). However, the effects
of IFN- on the inducible COX-2 mRNA have not been reported.
The objective of this study was to investigate the effect of steroid
hormone and IFN- on COX-2 and PGFS gene expression in different cell
types of bovine uterine endometrium. It was hypothesized that steroid
treatment of the cells would modify the effect of IFN- on PG
synthesis and on COX-2 and PGFS expression.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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was generously provided by Dr. R. M. Roberts (25).
Preparation and culture of cells
Bovine uteri from cows, at days 1–3 of the estrous cycle
(ovaries containing a corpus hemorrhagicum), were collected at the
slaughterhouse and transported, on ice, to the laboratory. Days 1–3
were selected because the stage of the estrous cycle can be accurately
determined from slaughterhouse material, because of the presence of the
corpus hemorrhagicum. This should decrease variability between uteri.
The endometrial epithelial and stromal cells were separated by a
modification of the procedure described by Fortier et al.
(26). Briefly, the two horns of the uteri were placed in sterile HBSS
containing 100 U penicillin, 100 µg streptomycin, and 0.25 µg
amphotericin per milliliter. The myometrial layers were dissected from
the two horns, and the horns were then inverted to expose the
epithelium. The inverted horns were first digested for 2 h in HBSS
with 0.3% trypsin at room temperature. At the end of incubation, the
digested horns were scraped slightly with forceps and then washed twice
in HBSS and further digested in HBSS with 0.064% trypsin III, 0.064%
collagenase II, and 0.032% deoxyribonuclease I for 45 min at 37 C, to
obtain the stromal cells. Once the cell suspension was collected, 10%
FCS was added to block the action of trypsin. The cell suspension was
centrifuged at 60 x g for 5 min. The pellets were
washed three more times with HBSS. The supernatants were pooled and
centrifuged at 1000 x g for 10 min and washed twice
with HBSS. Because most of the epithelial cells are in the form of
clumps after trypsin digestion, it is possible to separate them from
single stromal cells by low-speed centrifugation (60 x
g for 5 min). The pellet was then suspended in 20 ml RPMI
medium, containing 50 µg/ml gentamicin, and plated onto 100 x
20 mm Nunclon petri dishes (GIBCO, Grand Island, NY) and incubated at
37 C with 5% CO2-95% air for 3 h to allow for
attachment of contaminating stromal cells. At the end of incubation,
the floating cells were collected. After cell counting and viability
determination by trypan-blue exclusion, cells were plated onto
matri-gel-coated 100 x 20 mm Nunclon petri dishes. The stromal
cell suspension was plated onto 100 x 20 mm Nunclon petri dishes
for 3 h. The floating contaminating epithelial cells were washed
away by gentle pipetting, and the medium was replaced. At the time of
plating, the viability of both cell types was greater than 95%.
Hormone treatment
After confluence (about 7 days), cells were incubated in RPMI
medium supplemented with 5% dextran-charcoal treated FCS (DC-FCS) in
the presence or absence of E2 (10 nM), P4 (50
nM), or the combination of E2 (10 nM) and P4
(50 nM) for 4 days. Each group of cells was then incubated
for a further 48 h with the same steroid regimen and in either the
presence or absence of rbIFN- (10 and 100 ng/ml). At the end of the
culture, medium was collected for PG measurement, and the cells were
lysed with guanidinium isothiocyanate and stored at -70 C for RNA
isolation. Ten microliters of cell lysate were taken for DNA
measurement. DNA content was determined by the bisbenzimide fluorescent
dye method of Labarca and Paigen (27).
Isolation of total RNA and Northern blot analysis
Total RNA was isolated from the cultured cells by centrifugation
through a density gradient of 5.7 M cesium chloride. Forty
micrograms of total RNA was denatured at 56 C for 15 min,
electrophoresed in 1.2% agarose gel, and passively transferred to
Hybond nylon membranes by capillary blotting. The nylon membranes were
UV-cross-linked for 30 sec at 150 mJ in a UV chamber (Bio-Rad GS Gene
Linker; Bio-Rad Labs, Richmond, CA) and prehybridized for 4–6 h in
hybridization buffer at 55 C. Blots were hybridized with the
appropriate 32P-labeled probes (1 x 106
cpm/ml) for 16 h at 55 C; washed in 2 x saline sodium
citrate, 0.1% SDS at 60 C for 15–20 min; and then, successively, in
2 x saline sodium citrate, 0.1% SDS at 55 C for 15–20 min
twice. Autoradiography was performed with Kodak XAR-5 (Mandel
Scientific Company Ltd., Guelph, Ontario, Canada) and double
intensifying screen at -70 C for various exposure times. For
rehybridization with a different probe, blots were boiled for 3 min in
diethyl pyrocarbonate (DEPC)-treated H2O, containing 0.1%
SDS, and exposed to film overnight to check completeness of probe
removal. Autographic bands were scanned using Foto/Analyst (Fotodyne
Inc., New Berlin, WI), and the intensity of the autographic bands were
quantitated by the NIH-image program. The amount of mRNA loaded was
normalized using 28S mRNA.
Probes
Mouse cyclooxygenase-2, bovine PGFS, and human 28S complementary
DNA (cDNA) inserts were used as probes to detect COX-2, PGFS, and 28S
gene expression in cultured bovine uterine endometrial cells. The
probes included a mouse COX-2 cDNA (28), previously validated with
bovine tissues (29). A bovine PGFS cDNA probe was generated by RT-PCR.
Five micrograms of RNA, extracted from granulosa cells of bovine
preovulatory follicles (29), were reversed transcribed using avian
myeloblastosis virus RT (Pharmacia Biotech, Montréal, Canada) and
oligodeoxythymidine primers. For the PCR reaction, homologous primers
were designed from the published bovine PGHS sequence lung form (23).
The sense 25-mer primer 5'-TTAATGATGGCCACTTCATTCCTGT-3' corresponded to
region from +29 to +53 bp from the start codon, and the antisense
25-mer primer 5'-GAGTCAGTTCAAAGTCAAACACCTG-3' was from +841 to +865 bp
of the bovine PGFS lung form (23). The expected 837-bp PCR product was
subcloned into the pCR 2.1 vector (Invitrogen, Carlsbad, CA), and its
identity was confirmed by DNA sequencing using the T7 Sequencing Kit
(Pharmacia), which employs the Sanger dideoxy nucleotide chain
termination method (30).
RIA of PGF2 and PGE2
Concentrations of PGF2 were measured in 100-µl
aliquots of culture medium after 10-fold or 100-fold dilution with
assay buffer. Serial dilutions of medium samples (n = 3) were
parallel to the standard curve. The antibody was purchased from Cayman
Chemical Co. (Ann Arbor, MI); its cross-reactivity against PGFM, 6-keto
PGF1, PGD2, PGE2, and AA was
0.07, 6.1, 0.6, 0.2, and 0.002%, respectively, at 50% displacement.
The sensitivity of the assay was 62.5 pg/ml, and the intra- and
interassay coefficients of variation were 9.2 and 12.3%,
respectively.
Concentrations of PGE2 were measured directly in 10- or
100-µl aliquots of culture medium. The antiserum was purchased from
Assay Designs Inc. (Ann Arbor, MI); its cross-reactivity against
PGE1, PGF1, PGF2, and 6-keto
PGF1 was 70, 1.4, 0.7, and 0.6%, respectively. The
sensitivity of the assay was 40 pg/ml, and the intra- and interassay
coefficients of variation were 6.3 and 8.6%, respectively.
Endotoxin assay
The Limulus amebocyte lysate assay was used to measure the
endotoxin concentration in all reagents used in this experiment. The
protocol was provided by Sigma. The endotoxin contents of all reagents,
including rbIFN-, are lower than the detectable level by this method
(<0.1 ng/ml).
Statistical analysis
Each treatment was carried out using the cells from one uterus,
and each experiment was repeated with four different uteri. Effects of
treatment on PGF2, PGE2 production, and
COX-2 and PGFS expression of uterine cells were evaluated by
least-squares ANOVA. Treatments were analyzed in multifactorial design
(ANOVA), which included the main effects of experiments, cell type, and
hormone treatments. Simple contrasts were used to determine differences
between individual means. A probability of P < 0.05
was considered to be statistically significant.
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Results |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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content was
measured in the culture medium after incubating epithelial and stromal
cells with various doses of LPS for 24 h. Both epithelial and
stromal cells responded to LPS in a dose-dependent fashion (Fig. 1
). In the epithelial cells, LPS had a
much greater effect on PGE2 than on PGF2
production (Fig. 1a). LPS markedly increased the ratio of
PGE2 to PGF2 in epithelial cells. In the
stromal cells, LPS had a biphasic effect on PGF2
secretion (Fig. 1b). The stimulation of PGF2 and
PGE2 was similar, except at the 100-ng/ml dose.
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on PG production and PGE2 in the medium from the
untreated control cells were 11.6 ± 1.5 and 2.8 ± 0.65
ng/µg DNA, respectively. E2, alone or in the presence of P4,
significantly reduced PGF2 and PGE2
secretion (P < 0.01; Fig. 2, a and b). P4 alone increased
PGF2 (P < 0.02), but not
PGE2, secretion. E2, either alone or in the presence of P4,
decreased the ratio of PGE2 to PGF2
(P < 0.01; Fig. 2c). rbIFN- diminished
PGF2 production (P < 0.01) at both
concentrations in the control, E2, and P4-treated groups; however, no
effect of IFN was observed when the cells were treated with E2 and P4
together. rbIFN- decreased PGE2 secretion when the cells
were not treated with steroids. In the presence of P4, rbIFN-
increased PGE2 production; and in the presence of E2 or
E2+P4, rbIFN- had no effect on PGE2. IFN had no effect
on the PGE/PGF ratio when the cells were treated with E2 or P4+E2.
However, in the control and P4-treated cells, IFN significantly
increased the PGE/PGF ratio (P < 0.01).
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and
PGE2 in the medium from the control cells were 0.64 ±
0.08 and 7.6 ± 1.7 ng/µg DNA, respectively. Steroid hormones
had no significant effect on either PGF2 or
PGE2 secretion (Fig. 3, a and
b). The higher concentration (100 ng/ml) of rbIFN- increased
PGF2 production in the control and E2 groups (Fig. 3a)
and PGE2 secretion in all the groups (Fig. 3b). The ratio
of PGE2 to PGF2 was increased significantly
by rbIFN- in all groups, except the cells treated with E2 alone
(Fig. 3c).
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on COX-2 mRNA levels and PGE2. To determine
whether the regulation of PG production in endometrial cells by
steroids and rbIFN- was correlated with COX-2 gene expression, COX-2
mRNA levels were measured by Northern blot analysis. A 4.1-kb
transcript was detected by the mouse COX-2 cDNA probe in both cell
types (Fig. 4, a and c). In epithelial
cells (Fig. 4b), E2, alone and in combination with P4, decreased COX-2
mRNA (P < 0.01), whereas P4 alone had no effect.
IFN- attenuated COX-2 mRNA in a dose-dependent manner in the control
and P4-treated cells (P < 0.01). However, in the
presence of E2, IFN- had no effect on COX-2 expression.
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), steroid hormones had no significant effect
on the amount of COX-2 mRNA. IFN- significantly increased COX-2 mRNA
in a dose-dependent manner in all groups (P < 0.01);
however, the addition of E2 markedly decreased the induction of COX-2
gene expression by P4 (P < 0.01).
Effect of steroid hormones and IFN- on PGFS mRNA levels
PG F synthase (PGFS) is responsible for the reduction of
PGH2 to PGF2 and PGD2 to 9,
11ß-PGF2 (a stereoisomer of PGF2). To
determine whether the attenuation of PGF2 secretion in
epithelial cells, and the increase in ratio of PGE2 to
PGF2 in stromal cells, induced by rbIFN- is
correlated with PGFS expression in these cells, the changes in PGFS
mRNA levels induced by steroids and rbIFN- was determined by
Northern blot analysis. A 1.4-kb transcript was detected by a bovine
PGFS probe (Fig. 5, a and c). In
epithelial cells (Fig. 5b), steroid hormones alone had no significant
effect on PGFS expression. However, rbIFN- decreased PGFS mRNA in a
dose-dependent manner in all steroid treatment groups
(P < 0.01).
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), neither E2 nor P4 had any effect on PGFS
mRNA levels; however, the presence of both E2 and P4 seemed to
up-regulate PGFS mRNA, compared with the addition of P4 alone
(P < 0.05). rbIFN-, alone or in presence of steroid
hormones, decreased PGFS expression (P < 0.01). |
Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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is the luteolysin, secreted from the
endometrium, that is responsible for the regression of the CL at the
end of the estrous cycle in ruminants. IFN is the embryonic factor
responsible for preventing the secretion of PGF2 and,
possibly, increasing the secretion of PGE2, a luteotrophic
factor. Although it is known that both P4 and E2 are essential for the
induction of luteolysis, and that one action of IFN is to suppress the
action of E2 by down-regulating its receptor (10), the exact mechanism
of action of these hormones is still not completely understood.
The present study is the first to simultaneously examine the effects of
steroid hormones and IFN on PG secretion and on COX-2 and PGF synthase
gene expression in isolated endometrial cells. E2 significantly
decreased PGF2 and PGE2 production, whereas
P4 increased PGF2, but not PGE2, secretion
in epithelial cells. E2 and P4 had no effect on PGF2 and
PGE2 secretion by stromal cells. This is generally
consistent with the previous report by Asselin et al. (7).
In vivo, P4 increases uterine secretion of
PGF2 (31). E2 is generally thought to stimulate PG
synthesis, because administration of E2 to cows at midcycle (32) or to
P4-primed ovariectomized cows (33) stimulates PGF2
secretion. At the present time, it is not clear why E2 decreases
PGF2 secretion and prevents the P4-induced stimulation
in isolated cells in vitro but stimulates secretion in
vivo.
The decrease in PGF2 secretion induced by E2 in
vitro is probably caused by decreased COX-2 enzyme activity, given
that it is associated with a decrease in COX-2, but not PGFS, mRNA. P4
did not increase either COX-2 or PGFS mRNA, although it increased
PGF2 production; thus, the effect of P4 on
PGF2 production is probably not at the level of the gene
expression of these enzymes. This was also suggested by Smith et
al. (34). P4 may, however, act at the level of translation of
COX-2, because Charpigny et al. (24) have shown that ovine
endometrial COX-2 protein was highly induced by P4. Steroid hormone
treatment does not affect the amount of the COX-1 protein (24), and it
is unlikely that P4 acts via this constitutively expressed enzyme.
rbIFN- attenuated the secretion of both PGF2 and
PGE2 from epithelial cells. This agrees with previous
reports (12, 13, 14, 15, 16, 35). The decrease in PG secretion, brought about by
rbIFN-, was probably caused by the decrease in COX-2 mRNA. In the
presence of P4, rbIFN- enhanced the secretion of PGE2
and thus increased the PGE2/PGF2 ratio. This
might be explained by the inhibition of PGFS expression by rbIFN-,
whereby more of the precursor for PG synthesis will be available for
synthesis of PGE2. In contrast to its inhibitory effect on
PGF2 secretion in epithelial cells, rbIFN- markedly
enhanced PGF2 and PGE2 production in stromal
cells. IFN had a greater effect on PGE2 than on
PGF2, resulting in a net increase in the
PGE2/PGF2 ratio. The increase in PG
secretion was associated with an increase in COX-2 expression, and the
decrease in PGFS mRNA by rbIFN- may be responsible for the increased
PGE2/PGF2 ratio. The stimulation of
PGE2 by rbTP-1 (rbIFN-) has been previously reported in
bovine endometrial stromal cells (13) (36). Because PGE2 is
considered to be a luteoprotective agent (37) and stromal cells are a
predominant cell population in the endometrium, this induction of
PGE2 by rbIFN- may play an important role in the
maintenance of the CL.
Our results, and those of others (12, 13, 14, 15, 16, 35), differ from those
reported by Asselin et al. (36), who showed that rbIFN-
and recombinant ovine IFN- stimulated both PGF2 and
PGE2 in cultured bovine uterine epithelial cells. One
possible explanation of the different results is LPS contamination of
the IFN-, because gram-negative bacteria, including
Escherichia coli used to produce recombinant IFN-,
contain LPS in their cell membrane. LPS is a strong stimulator of PG
synthesis (especially PGE2) in many types of cells, such as
human monocytes (38), gingival fibroblasts (39), neutrophils (40), rat
peritoneal macrophages (41), and blood-derived macrophages of red deer
(42). The results presented in this study show that LPS is also a
powerful stimulator of PG synthesis in endometrial epithelial and
stromal cells. LPS increased PGE2 secretion more than
PGF2 in the epithelial cells, whereas the stimulation of
PGF2 and PGE2 were similar (except at 0.1
µg/ml) in stromal cells. In our study, all the reagents and the
rbIFN- were assayed for endotoxin, and the content was lower than
the limit of detection (<0.1 ng/ml) of the Limulus amebocyte lysate
assay. It might be important to screen recombinant products for
endotoxin content when used to investigate PG synthesis.
In conclusion, this study showed differential effects of E2, P4, and
rbIFN- in the regulation of PG production, and COX-2 and PGFS gene
expression in cultured bovine endometrial cells. Our results show that
E2 inhibited PGF2 and PGE2 production by
down-regulating COX-2 expression in epithelial cells. P4 increased
PGF2 secretion but did not up-regulate COX-2. rbIFN-
attenuated PGF2 and PGE2 in epithelial cells
and enhanced PGF2 and PGE2 in stromal cells
by down- and up-regulating COX-2 mRNA, respectively. The changes in the
ratio of PGE2 to PGF2, brought about by
rbIFN-, are associated with a decrease in PGFS mRNA abundance.
|
Acknowledgments |
|---|
; Dr. D. L. Simmens (Brigham Young University) for the
mouse COX-2 cDNA; Dr. G. Schultz for the 28S probe; and D. Rannou for
technical assistance. We are also very grateful for the assistance of
Dr. B. D. Murphy and his group. |
Footnotes |
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Received November 3, 1997.
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References |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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T. R. Bilby, A. Guzeloglu, S. Kamimura, S. M. Pancarci, F. Michel, H. H. Head, and W. W. Thatcher Pregnancy and Bovine Somatotropin in Nonlactating Dairy Cows: I. Ovarian, Conceptus, and Insulin-Like Growth Factor System Responses J Dairy Sci, October 1, 2004; 87(10): 3256 - 3267. [Abstract] [Full Text] [PDF]
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A. Guzeloglu, T. R. Bilby, A. Meikle, S. Kamimura, A. Kowalski, F. Michel, L. A. MacLaren, and W. W. Thatcher Pregnancy and Bovine Somatotropin in Nonlactating Dairy Cows: II. Endometrial Gene Expression Related to Maintenance of Pregnancy J Dairy Sci, October 1, 2004; 87(10): 3268 - 3279. [Abstract] [Full Text] [PDF]
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A. Guzeloglu, F. Michel, and W. W. Thatcher Differential Effects of Interferon-{tau} on the Prostaglandin Synthetic Pathway in Bovine Endometrial Cells Treated with Phorbol Ester J Dairy Sci, July 1, 2004; 87(7): 2032 - 2041. [Abstract] [Full Text] [PDF]
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A. K. Goff Steroid Hormone Modulation of Prostaglandin Secretion in the Ruminant Endometrium During the Estrous Cycle Biol Reprod, July 1, 2004; 71(1): 11 - 16. [Abstract] [Full Text] [PDF]
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A. Guzeloglu, P. Subramaniam, F. Michel, and W. W. Thatcher Interferon-{tau} Induces Degradation of Prostaglandin H Synthase-2 Messenger RNA in Bovine Endometrial Cells Through a Transcription-Dependent Mechanism Biol Reprod, July 1, 2004; 71(1): 170 - 176. [Abstract] [Full Text] [PDF]
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D. Boerboom, K. A. Brown, D. Vaillancourt, P. Poitras, A. K. Goff, K. Watanabe, M. Dore, and J. Sirois Expression of Key Prostaglandin Synthases in Equine Endometrium During Late Diestrus and Early Pregnancy Biol Reprod, February 1, 2004; 70(2): 391 - 399. [Abstract] [Full Text] [PDF]
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V. Emond, L. A. MacLaren, S. Kimmins, J. A. Arosh, M. A. Fortier, and R. D. Lambert Expression of Cyclooxygenase-2 and Granulocyte-Macrophage Colony-Stimulating Factor in the Endometrial Epithelium of the Cow Is Up-Regulated During Early Pregnancy and in Response to Intrauterine Infusions of Interferon-{tau} Biol Reprod, January 1, 2004; 70(1): 54 - 64. [Abstract] [Full Text] [PDF]
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K. Okuda, Y. Kasahara, S. Murakami, H. Takahashi, I. Woclawek-Potocka, and D. J. Skarzynski Interferon-{tau} Blocks the Stimulatory Effect of Tumor Necrosis Factor-{alpha} on Prostaglandin F2{alpha} Synthesis by Bovine Endometrial Stromal Cells Biol Reprod, January 1, 2004; 70(1): 191 - 197. [Abstract] [Full Text] [PDF]
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K. Tsuboi, A. Iwane, S. Nakazawa, Y. Sugimoto, and A. Ichikawa Role of Prostaglandin H2 Synthase 2 in Murine Parturition: Study on Ovariectomy-Induced Parturition in Prostaglandin F Receptor-Deficient Mice Biol Reprod, July 1, 2003; 69(1): 195 - 201. [Abstract] [Full Text] [PDF]
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 E. Madore, N. Harvey, J. Parent, P. Chapdelaine, J. A. Arosh, and M. A. Fortier An Aldose Reductase with 20alpha -Hydroxysteroid Dehydrogenase Activity Is Most Likely the Enzyme Responsible for the Production of Prostaglandin F2alpha in the Bovine Endometrium J. Biol. Chem., March 21, 2003; 278(13): 11205 - 11212. [Abstract] [Full Text] [PDF]
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J. Parent, C. Villeneuve, A. P. Alexenko, A. D. Ealy, and M. A. Fortier Influence of Different Isoforms of Recombinant Trophoblastic Interferons on Prostaglandin Production in Cultured Bovine Endometrial Cells Biol Reprod, March 1, 2003; 68(3): 1035 - 1043. [Abstract] [Full Text] [PDF]
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J. L. Cook, M. C. Shallow, D. B. Zaragoza, K. I. Anderson, and D. M. Olson Mouse Placental Prostaglandins Are Associated with Uterine Activation and the Timing of Birth Biol Reprod, February 1, 2003; 68(2): 579 - 587. [Abstract] [Full Text] [PDF]
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B. Wang, C. Xiao, and A. K. Goff Progesterone-Modulated Induction of Apoptosis by Interferon-Tau in Cultured Epithelial Cells of Bovine Endometrium Biol Reprod, February 1, 2003; 68(2): 673 - 679. [Abstract] [Full Text] [PDF]
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 S. J. Armstrong, Y. Zhang, K. G. Stewart, and S. T. Davidge Estrogen replacement reduces PGHS-2-dependent vasoconstriction in the aged rat Am J Physiol Heart Circ Physiol, September 1, 2002; 283(3): H893 - H898. [Abstract] [Full Text] [PDF]
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 S. Zervou, E. Karteris, E.W. Hillhouse, and R.W. Old Steroids mediate the expression of cytoplasmic and membrane-linked components in human myometrial cells Mol. Hum. Reprod., July 1, 2002; 8(7): 597 - 605. [Abstract] [Full Text] [PDF]
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J. A. Arosh, J. Parent, P. Chapdelaine, J. Sirois, and M. A. Fortier Expression of Cyclooxygenases 1 and 2 and Prostaglandin E Synthase in Bovine Endometrial Tissue During the Estrous Cycle Biol Reprod, July 1, 2002; 67(1): 161 - 169. [Abstract] [Full Text] [PDF]
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F. Doualla-Bell and A. E. Koromilas Induction of PG G/H Synthase-2 in Bovine Myometrial Cells by Interferon-{tau} Requires the Activation of the p38 MAPK Pathway Endocrinology, December 1, 2001; 142(12): 5107 - 5115. [Abstract] [Full Text] [PDF]
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 T. Sato, H. Michizu, K. Hashizume, and A. Ito Hormonal regulation of PGE2 and COX-2 production in rabbit uterine cervical fibroblasts J Appl Physiol, April 1, 2001; 90(4): 1227 - 1231. [Abstract] [Full Text] [PDF]
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J. K. Pru, B. R. Rueda, K. J. Austin, W. W. Thatcher, A. Guzeloglu, and T. R. Hansen Interferon-Tau Suppresses Prostaglandin F2{{alpha}} Secretion Independently of the Mitogen-Activated Protein Kinase and Nuclear Factor {{kappa}} B Pathways Biol Reprod, March 1, 2001; 64(3): 965 - 973. [Abstract] [Full Text]
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J. Liu, M. Antaya, A. K. Goff, D. Boerboom, D. W. Silversides, J. G. Lussier, and J. Sirois Molecular Characterization of Bovine Prostaglandin G/H Synthase-2 and Regulation in Uterine Stromal Cells Biol Reprod, March 1, 2001; 64(3): 983 - 991. [Abstract] [Full Text]
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 A. Kirschenbaum, D. R. Liotta, S. Yao, X.-H. Liu, A. P. Klausner, P. Unger, E. Shapiro, I. Leav, and A. C. Levine Immunohistochemical Localization of Cyclooxygenase-1 and Cyclooxygenase-2 in the Human Fetal and Adult Male Reproductive Tracts J. Clin. Endocrinol. Metab., September 1, 2000; 85(9): 3436 - 3441. [Abstract] [Full Text]
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E. Asselin and M. A. Fortier Detection and Regulation of the Messenger for a Putative Bovine Endometrial 9-Keto-Prostaglandin E2 Reductase: Effect of Oxytocin and Interferon-Tau Biol Reprod, January 1, 2000; 62(1): 125 - 131. [Abstract] [Full Text]
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J. Liu, M. Antaya, D. Boerboom, J. G. Lussier, D. W. Silversides, and J. Sirois The Delayed Activation of the Prostaglandin G/H Synthase-2 Promoter in Bovine Granulosa Cells Is Associated with Down-regulation of Truncated Upstream Stimulatory Factor-2 J. Biol. Chem., December 3, 1999; 274(49): 35037 - 35045. [Abstract] [Full Text] [PDF]
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C. W. Xiao, B. D. Murphy, J. Sirois, and A. K. Goff Down-Regulation of Oxytocin-Induced Cyclooxygenase-2 and Prostaglandin F Synthase Expression by Interferon-{tau} in Bovine Endometrial Cells Biol Reprod, March 1, 1999; 60(3): 656 - 663. [Abstract] [Full Text]
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) measurement by RIA. Data are normalized to the
DNA contents of respective wells and presented as fold stimulation of
the medium control.
