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The Journal of Clinical Endocrinology & Metabolism Vol. 84, No. 9 3344-3350
Copyright © 1999 by The Endocrine Society

Original Studies

Expression of Prolactin and Its Receptor in the Baboon Uterus during the Menstrual Cycle and Pregnancy1

Jonna Frasor, Christina A. Gaspar2, Kathleen M. Donnelly, Geula Gibori and Asgerally T. Fazleabas

Departments of Physiology and Biophysics (J.F., G.G., A.T.F.) and Obstetrics and Gynecology (C.A.G., K.M.D., A.T.F.), University of Illinois, Chicago, Illinois 60612

Address all correspondence and requests for reprints to: Asgi Fazleabas, Ph.D., Department of Obstetrics and Gynecology, University of Illinois, 820 S. Wood Street (M/C 808), Chicago, Illinois 60612.


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results and Discussion
 References
 
PRL is known to be a major secretory product of the human decidua. However, the physiological role of decidual PRL during the menstrual cycle and pregnancy has not been fully defined, primarily due to the lack of an appropriate nonhuman primate model for in vivo studies. Therefore, this initial study examined the expression of PRL and its receptor in the baboon uterus during the cycle and pregnancy. PRL and PRL receptor messenger ribonucleic acid expression were detected by semiquantitative RT-PCR, and protein was localized by immunocytochemistry. PRL was shown to be expressed in myometrial smooth muscle during the follicular phase by both RT-PCR and immunocytochemistry. Expression of PRL messenger ribonucleic acid and protein was first observed in the epithelial cells of the deep basal glands during the late luteal phase. With the onset of pregnancy, PRL expression increased steadily and was evident primarily in the decidual tissue. In contrast to PRL, its receptor was expressed at constant levels in both the myometrium and endometrium during the cycle. An increase in receptor expression was evident in both the decidua and placenta throughout pregnancy. In summary, these results demonstrate that the baboon uterus is a site of both PRL production and action during the cycle and pregnancy. These studies establish the baboon as a nonhuman primate model to investigate the potential roles of PRL in implantation and maintenance of pregnancy.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results and Discussion
 References
 
DECIDUALIZATION of the endometrium involves a series of morphological and molecular changes in which stromal fibroblasts differentiate into secretory decidual cells. In the human, stromal cells undergo a predecidual response during the last week of the menstrual cycle, whereas in nonhuman primates, decidualization requires the presence of a conceptus (1). One of the characteristic markers of decidualization in both the human and the baboon is the production and secretion of insulin-like growth factor-binding protein-1 (IGFBP-1). In the human, IGFBP-1 begins to be secreted by the stromal cells surrounding the spiral arteries during the late luteal phase, whereas in the baboon, IGFBP-1 is secreted from the glands in response to progesterone (2, 3). Stromal cell production of IGFBP-1 is up-regulated in the baboon in response to pregnancy, and in both the human and the baboon is correlated with the process of decidualiza-tion (4).

A second characteristic secretory product of the human decidua is PRL. The production of decidual PRL begins by day 22 of the cycle in the human and continues to increase throughout gestation (5). High levels of PRL are reached in the amniotic fluid, which then decrease with the onset of labor (6). Although high levels of PRL are measurable in baboon amniotic fluid (7), whether PRL is produced within the baboon uterus, as it is in the human, is as yet unknown. Therefore, this study was undertaken to characterize PRL production within the baboon uterus during the menstrual cycle and pregnancy. In addition, expression of the PRL receptor (PRL-R) was characterized to identify possible targets for PRL action within the uterus.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results and Discussion
 References
 
Tissue collection

Uterine tissue was obtained by hysterectomy or endometriectomy from adult female baboons (Papio anubis) at various points during the menstrual cycle or pregnancy (n = 2/day examined). The animal care committee of the University of Illinois approved all experiments and procedures. The stage of the cycle was determined by the following criteria: menstrual cycle history, sex skin tumescence, and serum levels of estradiol and progesterone (8, 9). The stage of pregnancy was confirmed by ultrasound and serum levels of CG, estradiol, and progesterone (10, 11). The myometrial tissue was separated from the endometrium for tissues obtained from cycling baboons. Tissue from pregnant baboons was divided into placenta and decidua. All tissue was either frozen in liquid nitrogen for ribonucleic acid (RNA) extraction or fixed in Bouin’s solution for paraffin embedding and immunocytochemistry (ICC).

RT-PCR

RNA was prepared from baboon endometrium, myometrium, decidua, and placenta at various days of pregnancy using Trizol reagent (Life Technologies, Inc., Gaithersburg, MD) according to the manufacturer’s instructions. For detection of PRL or PRL-R messenger RNA (mRNA), 1 or 3 µg total RNA, respectively, were reverse transcribed at 42 C using random hexamer primers (Pharmacia Biotech, Piscataway, NJ) and Moloney murine leukemia virus reverse transcriptase (Life Technologies, Inc.). Primers for PRL were designed to amplify a region of high homology between the human and rhesus monkey decidual PRL (5'-GCCCCCTTGCCCATCTGTCC-3' and 5'-AGAAGCCGTTTGGTTTGCTCC-3'). To detect expression of the long and short forms of the PRL-R, sense and antisense strand oligonucleotides corresponding a common extracellular domain and unique intracellular domains were used as previously described (12). In addition, two oligonucleotides (5'-CGTTCACCTTGATGAGAGCCAGT-3' and 5'-TCC-AAGGGTCCGCTGCAGTC-3') specific for ribosomal protein S16 mRNA were included in each PCR reaction as an internal control. Amplification was carried out using 2.5 U Taq DNA polymerase (Perkin Elmer Corp., Foster City, CA) and [{alpha}-32P]deoxy-CTP (Amersham Pharmacia Biotech, Arlington Heights, IL) for 30 cycles with an annealing temperature of 65 C. All PCRs were carried out in the linear phase of amplification. PCR products were electrophoresed on an 8% polyacrylamide gel and analyzed using a PhosphorImager (Molecular Dynamics, Inc., Sunnyvale, CA).

ICC

Six-micron sections of paraffin-embedded tissue were cut and mounted on poly-L-lysine-coated slides. Immunocytochemical localization of PRL was performed using a polyclonal antibody to recombinant human PRL at a dilution of 1:750 (Scripps Laboratory, San Diego, CA). A monoclonal antibody (T6; 12.5 µg/mL) to the rat PRL-R (provided by Dr. Paul Kelly) was used for ICC localization of the receptor. Immunostaining was visualized using avidin-biotin complexed to horseradish peroxidase (Vectastain ABC kit, Vector Laboratories, Inc., Burlingame, CA) and the chromogen diaminobenzidine (Sigma Chemical Co., St. Louis, MO). Negative controls included the substitution of he primary antibody with preimmune rabbit serum for PRL and mouse ascites fluid for PRL-R.


   Results and Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results and Discussion
References
 
PRL production in the baboon uterus

RNA obtained from endometrium and myometrium of cycling animals and from decidua and placenta of pregnant animals were analyzed for PRL expression by RT-PCR (Fig. 1AGo). PRL mRNA levels were quantitated and expressed relative to S16 mRNA levels in each sample (Fig. 1BGo). PRL mRNA could be detected in late luteal endometrium as well as follicular phase myometrium. The decidua expressed higher levels of PRL mRNA, which increased throughout pregnancy. Very low levels of PRL mRNA could also be detected in placental tissues.



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  		Figure 1. Detection of PRL mRNA by RT-PCR. A, Endometrium and myometrium from the follicular phase (FP) and the luteal phase (days 5, 10, and 12 postovulation) as well as decidua and placenta from days 29, 39, and 52 and at term of pregnancy were analyzed for PRL mRNA expression by RT-PCR. B, Quantitation of PRL mRNA levels relative to S16 mRNA levels.

 
To determine which cell types were producing PRL in the baboon uterus, PRL was localized by ICC using a polyclonal antibody to recombinant human PRL. In the endometrium, staining for PRL protein was absent during the follicular phase, but was evident in glandular epithelium and individual stromal cells during the late luteal phase (Fig. 2Go, A and B). In contrast, the myometrial smooth muscle stained positively for PRL during the follicular phase, but was absent in the luteal phase (Fig. 2Go, C and D). During pregnancy, both the decidua and placental syncytiotrophoblasts stained positively for PRL on days 39 and 59 and at term (Fig. 3Go). No staining was evident when preimmune serum was used in place of the primary antibody (data not shown).



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  		Figure 2. ICC localization of PRL during the menstrual cycle. Endometrium from the follicular (A) and luteal (B) phases as well as myometrium from the follicular (C) and luteal (D) phases were stained using a polyclonal antibody to recombinant human PRL. Magnification, x800.

 


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  		Figure 3. ICC localization of PRL during pregnancy. Decidua and placenta from day 39 (A and B) day 59 (C and D) of pregnancy and at the time of cesarean section (E and F) were stained using a polyclonal antibody to recombinant human PRL. Magnification, x800.

 
In the human, estradiol has been shown to stimulate pituitary PRL production, whereas progesterone is a potent stimulator of decidual PRL expression (13, 14). In contrast, myometrial PRL is down-regulated by progesterone (15). Our study suggests that regulation of uterine PRL by progesterone in the baboon is similar to that in the human. During the follicular phase, when low levels of progesterone are present, the myometrium expresses PRL mRNA and protein. However, during the luteal phase, as progesterone levels increase, myometrial PRL is down-regulated, and as progesterone levels rise, the glandular epithelium and stromal cells begin to produce PRL. However, it is the decidua tissue of pregnancy that produces high levels of PRL, which increase throughout pregnancy. Preliminary results in our laboratory have also shown that when baboon stromal cells are induced to decidualize in vitro, PRL mRNA expression is increased.

Although low levels of PRL mRNA were detected in the placenta, this tissue has not been shown to produce PRL. This may be attributed to decidual cells contaminating the placental tissue. In contrast, ICC staining for PRL was extremely high. This may be due to placental PRL-like proteins cross-reacting with the antibody or to the sequestration of PRL into the syncytiotrophoblast cells.

Expression of PRL-R in the baboon uterus

RNA isolated from endometrium and myometrium from cycling animals and from decidua and placenta of pregnant animals were examined for PRL-R expression by RT-PCR (Fig. 4AGo). In all tissues examined, only the long form of the PRL-R could be detected. Throughout the menstrual cycle, endometrial and myometrial PRL-R levels were relatively constant when normalized to S16 (Fig. 4BGo). PRL-R mRNA expression was also observed in both the decidua and placenta on day 39 and at term pregnancy.



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  		Figure 4. Detection of PRL-R mRNA by RT-PCR. A, Endometrium (E) and myometrium (M) from the follicular phase (FP) and from the luteal phase (days 5, 10, and 12 postovulation) as well as decidua (D) and placenta (P) from days 39 and term of pregnancy were analyzed for PRL-R mRNA expression by RT-PCR, B, Quantitation of PRL-R mRNA levels relative to S16 mRNA levels.

 
To determine which cells within these tissues express the PRL-R, ICC was performed using a monoclonal antibody to rat PRL-R. In tissue from cycling baboons, glandular epithelium and myometrial smooth muscle stained positively for PRL-R throughout the cycle (Fig. 5Go). Similarly, the decidua and placental syncytiotrophoblasts stained positively throughout pregnancy (Fig. 6Go). In addition, both the chorionic and amniotic fetal membranes demonstrated high levels of staining for the PRL-R at the time of delivery (data not shown). Again, no staining was observed when tissue sections were incubated with preimmune mouse ascites (data not shown).



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  		Figure 5. ICC localization of PRL-R during the menstrual cycle. Endometrium from the follicular (A) and luteal (B) phases as well as myometrium from the follicular (C) and luteal (D) phases were stained using a monoclonal antibody to rat PRL-R. Magnification, x800.

 


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  		Figure 6. ICC localization of PRL-R during pregnancy. Decidua and placenta from days 29 (A and B) and 71 (C and D) of pregnancy and at the time of cesarean section (E and F) were stained using a monoclonal antibody to rat PRL-R. Magnification, x800.

 
A recent study has shown that the human endometrium expresses the PRL-R in a pattern similar to that found for PRL: low in the proliferative and early secretory phases, increased in the mid- to late secretory phase, and further increased in the decidua of early pregnancy (16). The PRL-R has also been shown to be up-regulated in the human decidua and correlates with PRL gene expression (17). Furthermore, the PRL-R was expressed in human chorion, amnion, decidua, and placenta in late pregnancy (18). Similar to that in the human, baboon PRL-R expression in the endometrium was low during the menstrual cycle, but as decidualization progressed, both PRL and PRL-R expression increased. However, the PRL-R appears to be constituitively expressed in the myometrium during the cycle as well as in the placenta and fetal membranes during pregnancy.

The presence of both PRL and its receptor implies that PRL may play an autocrine/paracrine role within the uterus. However, what function PRL serves remains speculative. Its up-regulation at the time of decidualization suggests that PRL may play a role in preparing the endometrium for implantation, whereas its high level in amniotic fluid may indicate a role in the maintenance of pregnancy. Preliminary studies in the rat suggest that decidual PRL may play a critical role in the control of apoptosis during early pregnancy (19). Thus, one potential function of PRL may be to ensure cell survival during gestation. In further support of a role for PRL in the maintenance of pregnancy, Bethea et al. demonstrated that intrauterine infection leads to an increase in proinflammatory cytokines, a decrease in amniotic PRL, and the onset of labor in rhesus monkeys (20). In general, PRL has been shown to alter the immune response, with high levels being stimulatory and low levels being inhibitory (21). In addition, within the myometrium, PRL may cause an increase in smooth muscle cell number, as has been shown in vitro (22).

In conclusion, this study demonstrates for the first time that both PRL and the PRL-R are expressed in the baboon uterus. Furthermore, the regulation of PRL and PRL-R expression within the uterus is similar to that described in the human. These results indicate that the baboon may be an excellent model for in vivo studies related to the role of PRL in maintaining decidual integrity during gestation in the primate.


   Footnotes
 
1 This work was supported by NIH Grants HD-29964 (to A.T.F.) and HD-11119 (to G.G.) and a Lusto American Foundation Fellowship (to C.A.G.). This work was performed as part of the National Cooperative Program for Markers of Uterine Receptivity for Blastocyst Implantation. Back

2 Current address: Faculty of Pharmacology, University of Porto, 4000 Porto, Portugal. Back

Received September 17, 1998.

Revised April 2, 1999.

Accepted May 20, 1999.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results and Discussion
 References
 

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