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Muc1 and Glycan Expression in the Oviduct and Endometrium of a New World Monkey, Cebus apella¹

^a School of Medicine, University of Manchester, Manchester M13 0JH, United Kingdom ^b Unit of Reproduction and Development, Faculty of Biological Sciences, and ^c Unit of Human Reproduction, Department of Obstetrics and Gynaecology, School of Medicine, Catholic University of Chile, Casilla 114-D, Santiago, Chile ^d Department of Histopathology, Manchester Royal Infirmary, Manchester M13 0JH, United Kingdom

ABSTRACT

Cebus apella is a New World monkey that has a menstrual cycle of 18–23 days with implantation at approximately luteal Day 5. The aim of this study was to characterize by lectin- and antibody-labeling the distribution of Muc1 and associated glycans on the endometrial and oviductal epithelium during the luteal phase of the cycle. Endometrial histology showed a thin endometrium, with glands extending deeply into the myometrium. No obvious evidence of secretory differentiation in cells of either the superficial or the basal segments of glands could be obtained using a panel of antibodies and lectins that marked epithelial glycoprotein, and glycosylation changes observed in some other primate endometrial cycles were not observed in this study. Antibodies to human MUC1 were shown to cross-react with C. apella, and Muc1 was localized to the apical epithelial surfaces of both the endometrial and the tubal epithelium, with stronger expression in the latter. Again, no cyclic changes were noted. Antibodies specific to the isoform Muc1/Sec showed strong staining at the apical tubal epithelium, but no reactivity was detectable in the luminal epithelium of the uterus. This observation suggests differences between the two glycocalyces and could help to explain why C. apella embryos do not implant in this location.

implantation, monkey, Muc1, oviduct, uterus

INTRODUCTION

The uterus in mammals presents a barrier to implantation that is lifted during a specific receptive phase. Recent work has suggested that the epithelial cell-surface mucin MUC1 may contribute to this function in several species [1]. The New World monkey Cebus apella exhibits a menstrual cycle of approximately 18–23 days, with implantation on approximately luteal phase Day 5 [2]. Tubal implantation occurs spontaneously in nearly 1% of human pregnancies but is rarely observed in nonhuman primates. At present, no explanation accounts for the differences between endometrial and tubal epithelium, or for the virtual exclusion of tubal implantation in all mammals but the human. Comparing the molecular properties of these different Müllerian duct-derived epithelial cell surfaces may give important information in this regard. We have previously demonstrated expression of ß₃ and _v integrin subunits in both tubal and endometrial epithelia of women and C. apella [3]. Here, we present a comparison of Muc1 and glycan expression of tubal and endometrial epithelium, using lectin and antibody panels. In this way, we hope to gain insight into the mechanisms that protect this species from tubal implantation.

MATERIALS AND METHODS

Animals

The subjects were 12 sexually mature monkeys (C. apella) experiencing regular menstrual cycles of 18–22 days. Animals were caged individually under controlled conditions of 24–27°C, 70% humidity, and a 14L:10D photoperiod. Tap water was available ad libitum, and fresh and dry fruits, pelleted food, biscuits, and a cake containing milk, minerals, eggs, honey, and corn was provided daily. Tubal and endometrial tissues were obtained through a midventral laparotomy during the period from Day 1 to Day 10 of the luteal phase of the menstrual cycle. Areas comprising the fimbria (5), ampulla (9), and isthmus (9) were taken, but in some cases, it was not possible to obtain the entire tube because of adhesions from previous surgery. Samples from the uterus (11) were obtained by two longitudinal incisions. The dating protocol relied on daily ultrasound examination of the ovarian follicle during the periovulatory period and daily vaginal smears. Females were operated under ketamine-atropine anesthesia (i.m. injection of 10 mg/kg of Ketostop [Drag Pharma Invetec S.A., Santiago, Chile] with 0.04 mg/kg of atropine sulfate [Sanderson S.A., Santiago, Chile]). The surgery, care, and manipulation of the animals were in accordance with the ethical guidelines of our institution (Chilean Primate Center of the Catholic University of Santiago, Chile) and the Guide for the Care and Use of Laboratory Animals of the U.S. Department of Health and Human Services (NIH publication 86-23 revised 1985).

Histochemistry

After surgery, tissues were frozen or fixed in neutral-buffered formalin and embedded in paraplast. Sections of the endometrium were stained with elastic van Gieson stain to assess the morphology. All tissues were treated with antibodies against MUC1 core protein (BC3, 1:500 v:v), keratan sulfate (5D4, 1:1000 v:v), and NeuAc2,6-GalNAc (sialyl Tn, antibody B72.3; 1:1000 v:v) using a biotinylated second antibody (rabbit anti-mouse, 1:200 v:v) and either a high-molarity avidin-peroxidase detection system (5D4, B72.3) [4,5] or a Dako Catalysed Amplification System (BC3; Dako Ltd., High Wycombe, UK) according to the manufacturer's instructions. Staining was also carried out with a panel of biotinylated lectins (Table 1) [6], some of which were used with and without sialidase [5], and a high-molarity avidin-peroxidase revealing system as above. Cryosections were stained for MUC1 cytoplasmic domain (CT-1; a kind gift of Joy Burchill and Rosalind Graham, ICRF, London) [7], MUC1 VNTR (variable number tandem repeat, BC2, BC3; kindly donated by Peter Devine, University of Queensland) [8], MUC1/SEC secreted isoform (7H8/2, 7H10/5; a kind gift of D. Wreschner, Tel Aviv University) [9], and keratan sulfate (5D4; ICN, Basingstoke, UK) [10] using a standard immunofluorescence protocol. No staining was detected in any uterus or tube when the primary antibody was omitted or nonimmune rabbit serum was used. A ranking system of analysis was applied, whereby staining intensity was allocated a grade from 0 (negative) to 4 (intensely stained). Observations were made by two of the authors (C.J.P.J. and G.S.), and the inter- and intraobserver error was tested to assess the reproducibility of the system. A high degree of consistency was found between observers.

RESULTS

The major locus of glycan and mucin staining in both tubal and uterine tissue was the apical epithelial cell surface. For the purposes of this study, only this surface is described, because its properties are fundamental to blastocyst adherence. The immunostaining and lectin histochemistry of the apical surfaces of both tubal and uterine epithelial cells are summarized in Tables 2 through 5.

MUC1 in the Oviduct

Immunohistochemistry with antibody (CT-1) to the cytoplasmic domain of MUC1 revealed apical staining in the tubal epithelium in all areas during the luteal phase (Fig. 1, a–c). Some antibodies to the extracellular tandem repeat of human MUC1 (BC2, BC3), used at high concentration, bound to the apical cell surfaces in cryosections. The non-membrane spanning variant Muc1/Sec (detected using either of two monoclonal antibodies raised to the unique C-terminal peptide of the human homologue) was strongly expressed at the apical surface of the tubal epithelium (Fig. 2a).

View larger version (201K): [in this window] [in a new window]   FIG. 1. Immunofluorescence with antibody CT-1 to the cytoplasmic domain of MUC1 in the tubal (a–c) and endometrial (d–f) epithelium of tissues obtained on luteal phase days. Apical staining in different areas of the tube on Days 2 (a), 5 (b), and 7 (c) and binding to d) gland epithelium on Day 5 and to e) luminal and f) gland epithelium on Day 7 are shown. Note the variability in gland staining. Bar = 50 µm

View larger version (176K): [in this window] [in a new window]   FIG. 2. Immunofluorescence in the tube (a) and endometrium (b–c) using antibody 7H10/5 in tissues obtained on Day 5 of the luteal phase and their equivalent phase-contrast images (d–f). The antibody reveals the presence of the non-membrane spanning variant Muc1/Sec in a) the apical surface of the tubal epithelium, b) very weakly in the endometrial glands, but not in c) the endometrial luminal epithelium. Bar = 50 µm

Glycan Immunohistochemistry of the Oviduct

The distribution of keratan sulfate, as shown by the binding of 5D4, was very patchy in the oviduct (Fig. 3, a–c). In general, a trend toward increased staining in the isthmus, especially on Days 5–7 of the luteal phase, was observed. In some specimens, the apical surface of the ampulla and isthmus showed almost continuous staining at this stage in the cycle, whereas staining of the fimbriae showed a slight decline as the luteal phase advanced. In contrast, antibody B72.3 to sialyl Tn showed no binding to the tubal epithelial apical surface (Fig. 4a).

View larger version (96K): [in this window] [in a new window]   FIG. 3. Immunoperoxidase localization of keratan sulfate in the tube (a–c) and endometrium (d) using the antibody 5D4 in tissues obtained on Day 3 of the luteal phase. Keratan sulfate is present in the apical surface of a) fimbria and b) ampulla and more strongly in c) isthmus. Also note d) endometrial glands showing variable intensity in their levels of binding. Bars = 100 µm (a–c) and 200 µm (d)

View larger version (57K): [in this window] [in a new window]   FIG. 4. Immunolocalization of sialyl Tn in a) fimbria and b) endometrial glands using the antibody B72.3 in tissues obtained on Day 7 of the luteal phase. Sialyl Tn is present in endometrial glands only, with variable intensity. Bars = 100 µm (a) and 200 µm (b)

Lectin Histochemistry of the Oviduct

Most of the reagents used (Table 1) bound prominently to apical epithelial sites in the tubal epithelium, confirming the high density and compositional variety of the glycocalyx. This is illustrated for DBA and SBA in Figures 5, a–c, and 6, a and b, respectively. Fimbrial staining by most lectins tended to decrease with time apart from MAA, which showed a slight increase from Day 1 to Day 7 of the luteal phase (Table 2). In the rest of the tube, however, apical staining showed only minor fluctuations throughout the luteal phase. Variations in staining were observed between different specimens obtained on the same day and were at least as marked as those changes observed in different specimens as the luteal phase advanced. A general trend for glycan expression to be stronger at the isthmus than at the ampulla, however, was observed (Tables 3 and 4). This was particularly evident with UEA-1 and SBA. Several lectins bound strongly throughout the length of the tube; this was particularly striking with SNA, MAA, MPA, and L-PHA, with L-PHA showing some decrease with time. Staining with DBA was intense, with no detectable gradient along the tube or change with time during the luteal phase. AHA and ECA did not bind to tubal epithelium until sites were revealed by sialidase pretreatment, after which staining was strong, with ECA binding in a discontinuous fashion.

View larger version (119K): [in this window] [in a new window]   FIG. 5. Lectin histochemistry with DBA showing strong, uniform apical reactivity in tubal tissue (a–c) and reactivity in luminal and glandular epithelium of endometrium. a) Isthmus, luteal Day 1. b) Isthmus, luteal Day 6. c) Fimbria, luteal Day 7. d) Endometrium, luteal Day 1. Bars = 100 µm (a–c) and 200 µm (d)

Histopathology of the Endometrium

The endometrium in C. apella was shallow, with much of the gland length being embedded in myometrium (Fig. 7). Glands were lined by regular columnar epithelial cells, and cell morphology did not vary extensively during the luteal phase. Little secretory product was seen in gland lumina.

View larger version (156K): [in this window] [in a new window]   FIG. 7. Histology of the endometrium showing the stromal component (S) with the basal segments of the glands embedded in myometrium (M). Few secretions can be seen in gland lumina. Bar = 200 µm

Muc1 in the Endometrium

Muc1 reactivity could be detected in both luminal and glandular epithelium with the C-tail antibody CT-1 (Fig. 1, d–f). Glands showed considerable variability in their staining intensity. Staining was significantly lower in the endometrial luminal epithelium than in the tube (compare Fig. 1e with Fig. 1, a–c). In contrast to tubal epithelium, Muc1/Sec was not observed in endometrial luminal epithelium and was detectable only very weakly in endometrial glands (Fig. 2, b and c).

Glycan Immunohistochemistry of Endometrial Epithelium

In the endometrium, gland apical staining showed variable intensity in the binding of antibody to keratan sulfate (Fig. 3d). However, sialyl Tn was absent from the uterine luminal epithelium but present, to a variable extent, in endometrial glands (Fig. 4b).

Lectin Histochemistry of the Endometrium

Glycan expression varied considerably between different gland profiles and, often, between the superficial and deeper parts of the same gland as well. Variations were also observed between similarly dated specimens (Table 5). No marked and consistent changes could be related to progression through the luteal phase of the cycle, but a slight tendency was observed for staining of the glands to decrease between Day 1 and Day 5 of the luteal phase, as shown for SBA in Figure 6, c and d. As in the tube, sialidase pretreatment was required to reveal ECA-binding sites in endometrial glands, indicating the presence of a population of terminal sialic acid residues. With AHA, following sialidase pretreatment, no epithelial binding could be detected until Day 5 of the luteal phase, after which weak staining could occasionally be seen. This is in contrast to the ECA binding, which was present from Day 1. Postsialidase ECA and AHA staining represented the main observed difference in the glycan repertoire of the two epithelia (Fig. 8). The lack of lectin-stained secretory material in early and mid luteal phase endometrial gland lumina was notable (Figs. 5, 6, and 8).

View larger version (105K): [in this window] [in a new window]   FIG. 6. Lectin histochemistry with SBA showing strong apical reactivity in tubal and endometrial tissue. a) Fimbria on luteal Day 5. b) Isthmus on luteal Day 5 showing an increase in glycosylation. c) Endometrium, luteal Day 1. d) Endometrium, luteal Day 5. Variation was apparent in the staining intensity between gland profiles in the endometrium and between superficial and deep areas of the glands, but no consistent cyclical pattern was observed from Days 1–7 of the luteal phase. Little secretory product in gland lumina was apparent with any of the lectins used. Bars = 100 µm (a and b) and 200 µm (c and d)

View larger version (57K): [in this window] [in a new window]   FIG. 8. Binding of AHA after sialidase pretreatment to endometrium (a) and isthmus (b) on luteal Day 1 showing lack of stain in the endometrium at this stage in the cycle. Faint binding to the stroma (S) has occurred in both tissues. Bars = 200 µm (a) and 100 µm (b)

DISCUSSION

In C. apella, endometrial gland histology, glycosylation, and cyclical activity differ markedly from that observed in the human [10, 11] and baboon (Papio anubis) [5]. Little change occurs in the morphology of the glandular epithelium during the course of the luteal phase, and no evidence has been found of any conspicuous secretory activity. This is in agreement with the observed lack of cyclic echogenicity as detected by ultrasonography in the endometrium (A. Ortiz, personal communication). Wide variation in glycosylation is apparent, both within and between glands and between different specimens at the same stage of the cycle. The endometrial stroma is shallow, and glands extend deeply into the myometrium in this species. However, no consistent differences of morphology or glycosylation could be observed between the superficial and the basal gland segments.

In several species, including primates and nonprimates, Muc1 is expressed in endometrial epithelium [1, 12–17]. Sequence data indicate that C-terminal cytoplasmic sequences of Muc1 are highly conserved in primates and rodents [7], and most interspecies comparisons have relied on antibodies to this domain and, thus, have not included non-membrane spanning Muc1 variants. As expected, our data indicate cross-reactivity of human antibody with C. apella Muc1 in the C-terminal region. In general, little conservation of specific amino-acid sequences has occurred between species in the ectodomain, which exhibits a classical mucin property of tandem repeats rich in serine and threonine. One documented exception is the gibbon, in which substantial ectodomain sequence similarity occurs with the human [18], and the present findings of weak reactivity of C. apella Muc1 with antibodies to the human ectodomain suggests some similarity in this New World species as well. Furthermore, the observation that two monoclonal antibodies to the human form of the non-membrane spanning variant MUC1/SEC [9] cross-react with C. apella Muc1 suggests further similarities in the human and monkey gene sequences.

In rodents and pigs, Muc1 is expressed in uterine epithelium during the nonreceptive phase, but it disappears at the time of implantation [12, 17, 19, 20]. In human endometrial epithelium, MUC1 is expressed at relatively high levels during the implantation phase [15, 16], and evidence from in vitro implantation experiments suggests that expression is reduced locally at the site of blastocyst attachment to the epithelium [21]. Loss of Muc1 at implantation sites is also observed in the rabbit, where expression is strong in maternal epithelium but locally down-regulated by the embryo [14]. These observations are all consistent in indicating the loss of Muc1 at implantation, which is in keeping with its role as an inhibitor of cell-cell adhesion. In C. apella, our observations indicate a pattern of regulation in which the expression of Muc1 is weaker at the luminal endometrial epithelium—the site of implantation—than in the glands. Similar observations have been made in the baboon [13]. In C. apella, this is explained, at least in part, by the unique behavior of Muc1/Sec, which is absent from luminal epithelium but is expressed in glandular cells. In contrast, MUC1/SEC can be observed in both luminal and glandular endometrium in the human (unpublished data). This variant has not been studied in other species.

By the same argument, tubal epithelium should be antiadhesive, thus preventing ectopic implantation of embryos that, through delay in transport, develop and hatch intratubally. Accordingly, in C. apella, stronger Muc1 expression is observed at the apical surface of tubal epithelium than in the endometrium. In addition, MUC1 has been observed in human tubal tissue (unpublished data). The Sec variant exhibits a more pronounced gradient of expression, with strong reactivity in all tubal locations and little detectable reactivity in the endometrium.

Epithelial expression of keratan sulfate was observed in C. apella, both in the endometrium and the tube, as seen in the human, with particularly strong expression in the isthmus. Sialyl Tn, however, showed minimal binding to the tubal and uterine luminal epithelium, whereas variable expression was found in the endometrial glands. Similarly, in the human, sialyl Tn is confined to the glandular epithelium in the uterus [22] and is absent from tubal tissue (unpublished data). Both these glycans are associated with MUC1 in human endometrium, indicating that different glycoforms of MUC1 are present in different tissue compartments [22].

Lectin-binding analysis indicated that most classes of glycan detectable by the panel of lectins used here were present in both tube and endometrium. Sialic acid in both 2,3-(MAA) and 2,6-(SNA) linkage was widely distributed, often associated with subterminal ß-galactosyl and N-acetyl lactosaminyl residues, as shown by the increase in AHA and ECA staining after removal of sialic acid. Staining with WFA and SBA indicated the presence of terminal N-acetyl galactosamine, which was most intensely expressed in the gland and tubular epithelial cytoplasm at the beginning of the luteal phase, as was tri/tetraantennary nonbisected complex N-glycan, as shown by the binding of L-PHA. Abundant, though variable, amounts of clustered N-acetyl lactosamine termini were present throughout the tube and endometrium, as shown by the staining with DSA. Fucose residues, as demonstrated by UEA-1 staining, were most strongly expressed in the isthmic region, whereas DBA, which binds to structures related to fucosylated blood group A, was more uniformly distributed. Unlike in the human and baboon, which show highly cycle-regulated expression of DBA [5], binding of this lectin to the endometrium in C. apella remained fairly constant in the apical surfaces of the tubal and uterine epithelium. General similarities in glycan and mucin expression between the endometrium and tube suggest that their glycocalyces share similar antiadhesive properties.

Despite the above similarities, tubal implantation has only rarely been observed in nonhuman primates [23]. This implies that different epithelial adhesive properties must pertain in tubal and uterine sites, or that the interactions between human and nonhuman fertilized ova and their respective epithelia differ. Specific adhesion molecules, including integrin _vß₃, are expressed in both tubal and endometrial epithelia of women and C. apella [3, 4]. This might provide a molecular basis to explain the occurrence of tubal implantation in women, but it does not explain the absence of tubal attachment in C. apella. Our data indicate that Muc1 is expressed at a higher level in tubal than in uterine epithelium in this New World monkey, and one key contributory factor is the presence of the variant Muc1/Sec in the former tissue. This isoform associates strongly with the apical cell surface through its high-affinity binding to another splice variant, MUC1/Y [24]. Our results both confirm this association and suggest the likelihood that Muc1/Y is present in C. apella tissue.

Preliminary observations indicate that in women, MUC1/SEC is expressed at a higher level in the tubal epithelium (unpublished data). These findings suggest that both species show inhibitory characteristics at the tubal surface, with the protective mechanism apparently being more efficient in C. apella than in the human. The occurrence of tubal implantation may be associated with deficient expression of MUC1/SEC in the endosalpinx. The molecular interactions leading to attachment in normal implantation are unknown, however, and the mechanisms by which these interactions are modulated to allow implantation in the endometrium, but not in the tube, also require further elucidation.

ACKNOWLEDGMENTS

We gratefully acknowledge the expert assistance of Dr. Alejandra Ortíz in the care and management of the animals and with surgery. We thank Joy Burchill, Rosalind Graham, Peter Devine, and Daniel Wreschner for their generous gifts of antibodies and Dr. R.W. Stoddart (School of Medicine, University of Manchester) for helpful discussion.

FOOTNOTES

First decision: 24 October 2000.

¹ Support from FONDECYT Lineas Complementarias 8980008, WHO 98/LABENDO/RMG2, and RF 98024-98.

² Correspondence: John D. Aplin, Research Floor, St. Mary's Hospital, Manchester M13 0JH, UK. FAX: 44 161 276 6134; john.aplin{at}man.ac.uk

Accepted: January 8, 2001.

Received: August 2, 2000.

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