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Department of Cell Biology, Vanderbilt University School of Medicine (L.H.H., G.E.O.), Nashville, Tennessee 37232; the Department of Biochemistry and Molecular Biology, M. D. Anderson Cancer Center (D.D.C.), Houston, Texas 77030; and the Department of Cell Biology and Biochemistry, Texas Tech University Health Sciences Center (B.S.C.), Lubbock, Texas 79430
Address all correspondence and requests for reprints to: Dr. Loren H. Hoffman, Department of Cell Biology, Vanderbilt University School of Medicine, Nashville, Tennessee 37232. E-mail: loren.hoffman{at}mcmail
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Abstract |
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Muc1 is abundant on uterine epithelial cells of the mouse (6), and its expression during the periimplantation period is regulated by steroid hormones (4, 7). Estradiol stimulates expression of mouse endometrial Muc1, an effect that is inhibited by administration of progesterone. Just before embryo implantation, epithelial expression of Muc1 protein and messenger RNA (mRNA) decline to barely detectable levels, and this change is believed to contribute to generation of the receptive uterine state (4). It is probable that removal of the Muc1 barrier to trophoblast-epithelial membrane apposition allows ligand-receptor interactions important for embryo attachment, since implantation success rates after transfer of attachment-competent embryos into mouse uteri on different days of pseudopregnancy were inversely correlated with uterine Muc1 mRNA levels (4). Muc1 protein also appears to be reduced markedly during the receptive phase in pigs (8). This response is driven by steroid hormones and can be replicated in vitro (9). In contrast, human endometrial Muc1 mRNA and protein expression are stimulated by progesterone, with the highest levels reported at the time when implantation would normally occur, the midsecretory phase (10, 11). In baboons, endometrial Muc1 expression is likewise progesterone, rather than estrogen, dependent (12). In this case, however, differential regulation of Muc1 expression by luminal and glandular epithelial cells has been demonstrated; Muc1 expression decreases in luminal, but not glandular, epithelium of baboon uteri during the receptive phase (12).
A combination of structural and biochemical changes in uterine epithelium characterizes the receptive phase in rabbits (13, 14, 15), a species in which implantation is supported by progesterone alone in animals ovariectomized on the first day of pregnancy (16). Preliminary experiments performed in conjunction with the recent cloning of rabbit Muc1 indicated that its expression in the rabbit uterus is up-regulated by progesterone (17) as in primates (10, 12), instead of estrogen, as in rodents (4, 7). Thus, Muc1 expression is expected to be high during the progesterone-dominated receptive phase. This pattern of expression would conflict with the proposed antiadhesive or barrier role of Muc1 (4) with regard to implantation. However, it is possible that signals produced by embryos might locally reduce Muc1 at implantation. The potential role for blastocysts in modifying Muc1 expression by the endometrium remains unexplored. Implantation sites in the rabbit are readily visualized, and endometrial tissue from implant and nonimplant regions can be assessed separately, making this an ideal species in which to study the effect of blastocysts on the uterus. This study describes experiments performed to determine stage-specific and hormone-dependent expression of Muc1 in rabbit uterine epithelium and to analyze the influence of blastocyst apposition on this expression.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Northern blot analysis
RNA was isolated from tissue samples as previously described
(18). The integrity of each RNA sample was confirmed by electrophoretic
fractionation through formaldehyde-containing agarose gels (1.2%),
according to the method of Sambrook et al. (19), and
ethidium bromide staining. Poly(A)+ RNA was isolated from
pooled endometrium from six estrous rabbits and three individual
progesterone-treated rabbits by chromatography on
oligo(deoxythymidine)-cellulose (20). RNA concentrations were
determined spectrophotometrically by absorbance at 260 nm. The
A260/280 ratio for each sample was more than 1.8. RNA
samples [1 µg poly(A)+ or 20 µg total RNA] were
fractionated by electrophoresis through formaldehyde-containing agarose
(1.2%) gels, transferred to nitrocellulose membranes by capillary
elution in 20 x SSC (standard saline citrate), and UV
cross-linked. Membranes were prehybridized (30–90 min, 60 C) in a
solution of 1% SDS, 1 M NaCl, and 10% dextran sulfate.
Membranes were subsequently hybridized overnight (16–22 h) in the same
solution containing randomly primed 32P-labeled oCx [(SA,
1 x 108 cpm/µg), the 401-bp complementary DNA probe
to the tandem repeat domain of rabbit Muc1 (17)] and salmon sperm DNA
(100 µg/ml). After hybridization, membranes were washed twice for 5
min each time in 2 x SSC at room temperature, twice for 30 min
each time in 0.1 x SSC-0.1% SDS at 60 C, twice for 30 min each
time in 0.1 x SSC at room temperature. Autoradiographic exposure
was performed at -70 C using XAR-5 x-ray film with an intensifying
screen. The relative intensities of the resulting mRNA autoradiograms
were quantified with a computer-assisted image analysis system
(Bio-Image Visage 2000, Eastman Kodak Co., Ann Arbor, MI). Muc1
expression in total RNA was normalized to the signal for the
constitutively expressed ribosomal protein S2.
A constituitive probe, to control for RNA loading of Northern blots, was prepared by PCR amplification of a 625-bp Chinese hamster ovary (CHO)-B fragment (21, 22) cloned into pGEM3Z using SP6 and T7 primers and a PCR digoxigenin labeling mix (Boehringer Mannheim, Indianapolis, IN). The CHO-B transcript encodes the constitutively expressed ribosomal protein S2 (21, 22). The CHO-B plasmid construct was provided by Dr. Kelly Mayo of Northwestern University (Evanston, IL). The digoxigenin-conjugated PCR products were purified by agarose gel electrophoresis and isolated with a Qiaquick gel extraction kit (Quiagen, Santa Clarita, CA). After hybridization of blots, sites of digoxigenin-labeled probe were detected using alkaline phosphatase-conjugated sheep antidigoxigenin IgG (Boehringer Mannheim) and chemiluminescence as described previously (18). Between exposures to different probes, the blots were stripped by incubating three times for 15 min each time in a solution of 0.05 x SSC, 0.01 M EDTA, and 0.1% SDS, pH 8.0, at 100 C. Blots were then rinsed in 0.01 x SSC at room temperature and exposed to x-ray film to verify that all probe had been removed.
Immunofluorescence analysis
An affinity-purified rabbit antibody to the peptide CT-1, a
highly conserved sequence at the C-terminus of Muc1 (23), was prepared
as described previously (4). The antibody was biotinylated using
biotinamidocaproate-N-hydroxysylfosuccinimide ester
according to manufacturer’s instructions (Sigma Chemical Co., St.
Louis, MO). A ratio of approximately 2 mol biotin/mol IgG was
determined using the avidin-4'-hydroxyazobenzene-2-carboxylic acid
assay (24). Cryostat sections, 4 µm thick, were fixed briefly in cold
methanol, then blocked with 1% (wt/vol) BSA and 1% (wt/vol) fish
gelatin in PBS. Endogenous biotin, biotin receptors, or avidin-binding
sites in tissue were blocked using avidin/biotin-blocking reagents
(Vector Laboratories, Burlingame, CA). Sections were incubated with
biotinylated anti-Muc1 (CT-1) at a concentration of 10 µg/ml,
followed by fluorescein-conjugated avidin (Vector). Control sections
were reacted with biotinylated anti-Muc1 preabsorbed with CT-1 peptide
(10:1 molar ratio of CT-1 to IgG). CT-1 peptide (CSSLSYTNPAVAATSANL)
was synthesized by the Synthetic Antigen Core Facility at M. D.
Anderson Cancer Center (Houston, TX). Sections were viewed under
epifluorescence optics, and endometrial regions and cell types were
identified using phase contrast microscopy.
Coculture of uterine epithelial cells with trophoblastic
vesicles
Reagents and media for cell isolation and culture were obtained
from Sigma Chemical Co. unless indicated otherwise. Epithelial cells
were isolated from uteri of 4-day PSP females as described previously
(25). Briefly, uteri were everted and incubated in 0.25% (wt/vol)
trypsin (type III) and 0.05% (wt/vol) bacterial protease (type XIV) in
calcium- and magnesium-free Hanks’ buffered salt solution for 90 min
at 37 C with continuous oscillation. Cell clusters (3–15 cells) were
collected from the resulting cell suspension by unit gravity
sedimentation for 5 min and assessed for cell number and viability
index (trypan blue exclusion). Clusters were suspended in DF culture
medium [HEPES-buffered DMEM-Ham’s F-12 medium (1:1) without phenol
red] containing 10% (vol/vol) dextran charcoal-treated FBS (HyClone
Laboratories, Logan, UT) and 1% antibiotic-antimycotic solution
(A-7292, Sigma). Epithelial cells were seeded onto Millicell-CM culture
inserts (30-mm diameter; Millipore Corp., Bedford, MA) at a density of
6 x 105 cells/insert. Insert membranes had been
coated with 125 µl Matrigel (Collaborative Biomedical Products,
Bedford, MA) and type I collagen (Celtrix Pharmaceuticals, Santa Clara,
CA) in a 1:2 ratio (vol/vol). Culture medium was then added to the
basal chamber, and dishes were placed in a humidified incubator at 37 C
in 5% CO2-95% air. On day 1 (24 h in culture), inserts
were rinsed to remove unattached cells, and the medium was replaced
with serum-free DF culture medium containing insulin, transferrin,
selenious acid, linoleic acid, and BSA (Collaborative Biomedical) and
1% antibiotic-antimycotic solution.
Blastocysts were obtained by flushing 6.75-day PG uteri with culture medium containing 1 mg/ml BSA, and the oviduct-derived blastocyst coatings (14) were removed by dissection. Trophoblastic vesicles were prepared using microscissors to repeatedly cut blastocysts to produce vesicles with the trophoblast oriented externally. Over 100 vesicles were obtained per female (6–12 blastocysts). These vesicles recovered their spherical shape during an 18-h incubation in serum-free DF medium containing 5 mg/ml BSA. At that time, any irregularly shaped vesicles (typically 5–15%) were removed, and the remainder were treated briefly with DF medium containing 400 U/ml deoxyribonuclease I (Worthington Biochemical, Freehold, NJ). Six to 10 vesicles were seeded onto each epithelial monolayer on day 3 of culture. The medium was supplemented with progesterone (1 µM) for half of the wells used. Control cultures were incubated with culture medium lacking vesicles. After 24 h of coculture, the regions of epithelial cell surface apposed to vesicles were outlined using a series of small needle punctures, loose vesicles were removed, and the epithelium was rinsed in PBS and fixed with cold methanol. In a few cases, the attaching vesicles remained adherent to the monolayer throughout the processing. Muc1 was localized on cryosections as described above. This experiment was carried out three times using uterine epithelial cells isolated from 4-day PSP females, and blastocysts were collected on day 6.75 PG. Cryosections were prepared from 2–3 vesicle-apposed regions of epithelial monolayers and a similar number of nonapposed regions for each experiment.
To examine potential effects of soluble trophoblastic products, conditioned medium was collected after 24 h of embryo culture. One batch of medium was obtained from 8 intact blastocysts (1 ml culture medium) and a second from 60 trophoblastic vesicles prepared from 5 blastocysts (500 µl medium). Conditioned media were placed in apical chambers of culture inserts with epithelial cell monolayers; the cultures were terminated after 24-h incubation for processing as described above.
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Results |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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shows that a single 2.4-kb Muc1
message was detectable in poly(A)+ RNA from estrous
animals. The steady state levels of Muc1 message were increased 10-fold
when estrous animals were treated with progesterone for 5 days (Fig. 1a). As shown in Fig. 1b, Muc1 message was detectable in total RNA from
kidney and uterine endometrium from an estrous rabbit and was not
detectable in ovary and liver. Muc1 levels were elevated 2- and 6-fold
in PSP females on days 4 and 6.75, respectively, and 30-fold in
preimplantation-stage uteri (6.75 days PG). Minimal differences were
apparent between blastocyst-containing and blastocyst-free regions at
this time. However, 12 h later, at the time of implantation,
i.e. day 7.25 PG, the 30-fold increase in Muc1 expression
was sustained in the nonimplant regions of the uterine endometrium and
was dramatically reduced in the endometrium from implantation sites
(Fig. 1a), comparable to levels noted in 6.75 day PSP endometrium.
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). Between estrus and day 4 of PSP,
rabbit endometrial cells proliferated extensively, resulting in the
formation of mucosal folds lined by columnar epithelium (cryptal
epithelium), similar to the luminal epithelium (26, 27). Short glands
were located deep in the crypts against the myometrium. Some increase
in the length of the folds occurred between 4 and 6.75–7 days PSP or
PG (26). Muc1 distribution was similar at 4 and 6.75 days of PSP (not
shown), with prominent apical staining of luminal and cryptal cells and
a weaker reaction in glandular cells. In both blastocyst-free (Fig. 2b)
and blastocyst-containing regions at 6.75 days PG, Muc1 staining was
similar to that seen at the PSP stages examined. Similarly, at 7.25
days PG (Fig. 2, c and d), approximately 6 h after blastocyst
attachment was initiated (14, 28), Muc1 staining in nonimplant regions
was comparable to that at earlier stages (4 and 6.75 days PSP, 6.75
days PG). At implantation sites, however, a marked reduction in
staining was apparent. The luminal epithelium closely apposed to
blastocysts had either patchy or no Muc1 staining, whereas the
underlying cryptal epithelium had moderate immunofluorescence (Fig. 2, e and f). Glandular staining was extremely weak in both implant and
nonimplant regions on day 7.25 PG. Controls, in which the anti-CT-1 was
preabsorbed with excess antigen, exhibited no specific immunostaining
at any reproductive stage.
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, a and b)
and without (not shown) progesterone in the culture medium. As with
implantation sites in vivo, where trophoblastic vesicles
were in close apposition to uterine epithelial cells, the intensity of
immunostaining was considerably reduced. In the few samples in which
vesicles had attached and trophoblast remained adherent to the
monolayer, the epithelial cells immediately adjacent to the attachment
site stained weakly or not at all (Fig. 3, c and d). This pattern of
immunostaining was apparent in two experiments (two of two and three of
three vesicle sites), whereas a vesicle-related reduction in Muc1
immunostaining was less conclusive in the third experiment (one of
three sites with reduced staining). Epithelial immunostaining was not
modified by inclusion of blastocyst-conditioned medium in the apical
chamber (data not shown).
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Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Immunofluorescence analysis of Muc1 expression in cultured epithelial cells failed to detect changes with progesterone treatment. This is perhaps not surprising, as day 4 PSP epithelial cells cultured under identical conditions exhibited synthesis of progesterone-dependent uterine secretory proteins (uteroglobin and haptoglobin), but further increases with progesterone treatment were not obtained (25). Nonetheless, cell monolayers derived from estrous females, which would have had minimal exposure to progesterone in vivo, failed to produce immunodetectable quantities of these endometrial glycoproteins. An earlier study reported progesterone-dependent increases in cell-associated sialomucoglycoproteins when epithelial cells derived from immature rabbit uteri were employed (36). Assuming that Muc1 would have been a major component of the sialomucoglycoprotein fraction assayed, the difference in response to progesterone reported in that study and the findings reported here could be due to 1) the developmental state of endometrium employed, 2) the differing methods of isolation and cell culture, or 3) immunofluorescence vs. biochemical assay of mucin expression. Alternatively, mucins other than Muc1 may be progesterone induced in vitro. In this regard, it has been shown that Muc1 accounts for only approximately 10% of the total mucin-type glycoconjugates in mouse uterine epithelia (37). Moreover, in addition to Muc1, Muc6 recently has been detected in human uterine epithelia (38).
Rabbit blastocysts appear to require several hours of contact with the endometrium before attachment can take place. This is evidenced by the requirement for a more than 9-h period of blastocyst apposition before significant increases in endometrial vascular permeability can be detected (39, 40). Furthermore, Hohn and Denker (41) reported that in vitro attachment of rabbit blastocysts to endometrial explants required that they be physically immobilized in close apposition during the coculture period. In the trophoblastic vesicle-uterine epithelial cocultures employed in our study, only limited attachment occurred in the first 24 h of apposition. It appears that during this time in vitro, as well as in vivo, the embryo induces down-regulation of Muc1. Although the current study does not address the nature of embryo-derived signals that may result in decreased endometrial levels of Muc1 mRNA, a potential candidate might be blastocyst-derived estradiol. The hypothesis that steroids of embryonic origin play a role in rabbit implantation has been controversial. Nonetheless, the enzymatic capacity for estrogen synthesis, accumulation of maternal estrogen, and local stimulation of endometrial estrogen conversion from steroid precursors by implantation stage blastocysts have each been reported for this species (reviewed in Ref.42).
We cannot dismiss the possibility that additional reduction of Muc1 occurs by localized proteolytic cleavage of the extracellular domain of the mucin, because the trophoblast of implanting rabbit blastocysts is known to elaborate several proteases (14). Although the antibody used in this study is directed against the cytoplasmic domain of Muc1, this segment is readily removed from the apical cytoplasm after cleavage of the extracellular domain (37). If there is a role for proteolysis, this may take place only in the immediate vicinity of trophoblast knobs, as blastocyst-conditioned medium had little or no effect discernible by immunostaining of epithelial monolayers. The local effect of blastocyst-derived vesicles in vitro is comparable to findings with intact implantation sites in which the immediately adjacent luminal epithelium and upper crypt cells exhibited decreased Muc1 immunostaining, whereas cells deeper in the crypts were less obviously affected.
In summary, the results of this investigation demonstrate that Muc1 is present on the surface of rabbit endometrial epithelial cells, and its expression is up-regulated by progesterone. Muc1 expression increases throughout the 7 days following ovulation, reaching high levels just before and during implantation. This potentially antiadhesive mucin is also regulated by blastocysts; during implantation, the presence of blastocysts results in a localized down-regulation of Muc1 expression. To our knowledge, this represents the first report of Muc1 regulation by blastocysts in the endometrium of any mammal.
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Acknowledgments |
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Footnotes |
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Received September 2, 1997.
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References |
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-dihydroprogesterone, and estradiol-17ß in
pregnant and pseudopregnant rabbits: evidence for postimplantation
recognition of pregnancy. Biol Reprod 23:1014–1019[Abstract]
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