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The Journal of Clinical Endocrinology & Metabolism Vol. 83, No. 2 509-513
Copyright © 1998 by The Endocrine Society

Original Studies

Identification of Progesterone Receptor in Human Subcutaneous Adipose Tissue

Susan N. O’Brien, Brenda H. Welter, Kimberly A. Mantzke and Thomas M. Price

Greenville Hospital System/Clemson University Biomedical Cooperative Research Program, Clemson University, Clemson, South Carolina 29634

Address all correspondence and requests for reprints to: Susan N. O’Brien, Greenville Hospital System/Clemson University Biomedical Cooperative, Clemson University, 124 Long Hall, Clemson, South Carolina 29634-5112.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Sex steroids are postulated to play a role in adipose tissue regulation and distribution, because the amount and location of adipose tissue changes during puberty and menopause. Because of the nature of adipose tissue, receptors for the female sex steroids have been difficult to demonstrate. To date, estrogen receptor messenger RNA and protein have been identified in human subcutaneous adipose tissue, but the presence of progesterone receptor (PR) has not been reported. In this study, we demonstrate PR message by Northern blot analysis in RNA isolated from the abdominal subcutaneous adipose tissue of premenopausal women. These preliminary studies revealed that PR messenger RNA levels are higher in the stromal-vascular fraction as opposed to the adipocyte fraction. Western blot analysis demonstrates both PR protein isoforms (human PR-A and human PR-B) in human subcutaneous adipose tissue. Using an enzyme-linked immunosorbent assay, total PR could be quantitated. These studies substantiate that sex steroid receptors are present in human adipose tissue, thereby providing a direct route for regulation of adipose tissue by female sex steroids.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
SEX steroids are postulated to influence adipose tissue regulation and distribution, because changes in fat distribution coincide with onset of ovarian production of estrogen and progesterone during puberty and with cessation of hormone production during menopause (1). Women typically demonstrate a gynoid or lower body fat distribution, whereas women with excessive androgens and glucocorticoids manifest an android or upper body fat distribution (2). Android adipose tissue distribution in women has been associated with an increased risk of diseases, including coronary artery disease (3), adult-onset diabetes mellitus (4), and endometrial cancer (5). Although clinical observations suggest that sex steroids influence adipose distribution, controversy exists as to whether sex steroids mediate these effects directly or indirectly in human adipose tissue. The dispute has been fueled by technical difficulty in detecting sex steroid hormone receptors in human adipose tissue (6, 7).

Estrogen receptor (ER) messenger RNA (mRNA) and protein have been identified in human subcutaneous adipose tissue (8, 9). We have reported the presence of higher ER mRNA levels in the adipocyte fraction of adipose tissue compared with ER mRNA levels in the stromal-vascular portion (8). In this study, we demonstrated the presence of progesterone receptor (PR) mRNA and protein in subcutaneous adipose tissue of premenopausal women and examined the distribution of PR message in the two cell fractions.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects

Subcutaneous adipose tissue was obtained from five premenopausal women undergoing elective adominoplasty with an average age of 43 ± 4 yr and mean body mass index of 26.8 ± 5.5 kg/m2. The included subjects were not taking exogenous hormones and were free of neoplastic, inflammatory, or autoimmune disease. All subjects signed an Institutional Review Committee-approved consent form (Greenville Hospital System) before surgery for use of tissue in research.

Tissue acquisition and processing

A portion of tissue was frozen immediately in liquid nitrogen for subsequent Western blot analyses and enzyme-linked immunosorbent assay (ELISA). Fresh adipose tissue was processed into adipocyte and stromal-vascular fractions as previously described (8). Both fractions were frozen in liquid nitrogen for Northern blot analyses.

RNA isolation and Northern blot analysis

Total RNA was isolated from whole abdominal adipose and myometrium using an RNeasy kit (Qiagen, Santa Clarita, CA) according to the manufacturer’s directions. Five micrograms of RNA was electrophoresed on a 1.2% denaturing agarose gel. The integrity of RNA was assessed by ethidium bromide staining of the gel. RNA was transferred to nylon by capillary blotting and fixed by ultraviolet cross-linking and vacuum baking. The filter was hybridized overnight at 65 C using a 32P random-prime labeled complementary DNA (cDNA) for human PR (10) added to prehybridization solution (7% SDS, 0.25 M sodium phosphate buffer, pH 7.2). Northern blots were washed at room temperature with 2x SSC and 0.1% SDS for 15 min followed by 2x SSC and 0.1% SDS for 15 min at 65 C and then exposed to film.

For comparison of mRNA from the stromal-vascular and adipocyte cell fractions, total RNA was isolated as described above. Equal amounts of RNA from each fraction were denatured and applied to a nylon membrane housed in a slot-blot manifold. RNA was fixed and hybridized as described above. The autoradiograph was quantitated by scanning two-dimensional densitometry. The filter was then stripped and rehybridized with a 1.076-kilobase (kb) fragment of the mouse cytoplasmic ß-actin gene (Ambion, Austin, TX). Following densitometry, PR values were normalized with ß-actin values. The difference between the ratio of PR to ß-actin densitometry values for adipocytes compared with stromal-vascular cells in the five subjects were compared with a paired sample t test.

Ammonium sulfate precipitation and Western blot analysis

Frozen abdominal adipose tissue was ground with mortar and pestle in liquid nitrogen, added to TEMMG buffer (10 mM Tris-HCl, 1.5 mM EDTA, 12 mM monothioglycerol, 10 mM sodium molybdate, 10% glycerol) with protease inhibitors (10 µg/mL leupeptin, 1 mM phenylmethylsulfonyl fluoride, 10 µg/mL aprotinin, 1 µg/mL pepstatin), and homogenized on ice. As a positive control, uterine tissue was prepared in the same manner as adipose tissue. Following centrifugation for 20 min at 16,000 x g, the layer between the floating lipid and pellet was removed. Ammonium sulfate was added to an aliquot of the cytosol to 30% saturation and rotated overnight at 4 C. The mixture was centrifuged at 3000 x g for 30 min. Precipitates were resuspended in TEMMG plus SDS sample buffer and boiled for 2 min before loading.

Samples were electrophoresed on a 7.5% polyacrylamide gel and transferred to polyvinylidene difluoride (Bio-Rad Labs., Hercules, CA). The membrane was incubated with rabbit antihuman PR (C19, Santa Cruz Biotechnology, Santa Cruz, CA) overnight at 4 C. As a second control, duplicate lanes were incubated with rabbit sera in place of the primary antibody. The membrane was washed and incubated with secondary antibody, peroxidase-conjugated goat antirabbit IgG (Cappel, ICN Pharmaceuticals, Costa Mesa, CA). Proteins were detected using an Enhanced Chemi Luminescense Western blotting detection system (Amersham, Buckinghamshire, England) according to the manufacturer’s directions.

ELISA

Frozen tissue was prepared in the same manner as for Western analyses. Protein was quantitated using Bradford analysis (BioRad). A 96-well plate was coated with a mixture of PR antibodies from NeoMarkers, PR antibodies 3, 4, 5, and 7 (Labvision, Freemont, CA) diluted to 1.5 µg/mL in 0.1 M sodium carbonate buffer (pH 9.3) at 100 µL/well. All subsequent volumes were 100 µL. The plate was incubated overnight at 4 C and then washed with PBS with 0.1% BSA and 0.05% Tween-20 (PBS-BSA-T) and blocked with 3% BSA in PBS. PR standard (Hormone Receptor Laboratory, Louisville, KY) at concentrations of 0, 3.75, 7.5, and 15 fmol/mg protein or 1 mg sample diluted with TEMMG were added to quadruplicate wells and incubated overnight at 4 C. After washing, a rabbit polyclonal PR antibody, C19, diluted to 0.5 µg/mL in PBS-BSA-T was added to triplicate wells. For a blank, one well included only PBS-BSA-T, without the primary C19 antibody. The plate was incubated overnight at 4 C. Biotinylated goat antirabbit IgG (Kirkegaard & Perry, Gaithersburg, MD) diluted 1:5000 in PBS-BSA-T was added to each well and incubated 1 h at room temperature. ImmunoPure Ultra-Sensitive ABC (Pierce, Rockford, IL) reagents were prepared according to the manufacturer’s directions, added to each well, and incubated 30 min at room temperature. Color developer (Horseradish Peroxidase Substrate Kit, BioRad) was added, and color development was measured after 1 h at 405 nm. Each sample was assayed in triplicate in three separate assays. The intraassay coefficient of variation (COV), calculated from values for the 7.5 fmol/mg protein standard was 4.5%. The interassay COV (11%) was calculated from the same standard values.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Figure 1Go shows the PR protein by Western blot analysis after ammonium sulfate precipitation in myometrium and abdominal adipose tissue. The human PR-B (hPR-B) isoform appeared at approximately 116 kilodaltons (kDa) and was identical in size to that found in the myometrium. The hPR-A isoform was located at approximately 92 kDa in adipose tissue, which was slightly greater than the predominant hPR-A band found at 83 kDa in the myometrium. A less intense third band in the myometrium was seen at 92 kDa corresponding to the hPR-A of the adipose tissue. Bands of these sizes were not detected in negative controls.



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  		Figure 1. Western blot analysis for hPR protein after ammonium sulfate precipitation. In myometrium (lane 1, 40 µg total protein), hPR-B isoform was identified at 116 kDa, whereas hPR-A isoform was primarily seen at 83 kDa, with a less intense band at 92 kDa. In adipose tissue (lane 2, 2 mg total protein), hPR-B isoform was identified at 116 kDa, whereas hPR-A isoform was primarily seen at 92 kDa. Control lane (lane 3, 2 mg adipose total protein) showed no specific bands when rabbit serum was used in place of primary antibody. A control lane with myometrial total protein also showing no specific binding is not shown.

 
In Fig. 2Go, Northern blot analysis of total RNA isolated from abdominal adipose tissue demonstrating the same size transcripts as seen in RNA isolated from myometrium is shown. The most prominent bands corresponded to sizes of 11.4, 6.1, 4.5, and 2.9 kb.



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  		Figure 2. Northern blot analysis of hPR mRNA in adipose tissue (adip) and myometrium (uterus). Five micrograms total RNA was separated by denaturing gel electrophoresis, applied to nylon, and probed with a randomly primed labeled hPR cDNA. Bands of identical sizes were predominantly seen at 11.4, 6.1, 4.5, and 2.9 kb.

 
Figure 3Go shows the levels of PR protein in abdominal adipose tissue from five subjects and the level in myometrium from one subject as determined by ELISA. PR protein levels in adipose tissue varied from approximately 3–8 fmol/mg total protein and were approximately 100-fold less than those found in myometrium. The insert shows a typical standard curve used for the PR ELISA.



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  		Figure 3. Quantitation of PR protein levels by ELISA in adipose tissue of five subjects and from one myometrium sample. SD bars represent variation for each subject within three separate assays. Insert, A typical standard curve using PR standards as described in Subjects and Methods.

 
Figure 4Go shows PR mRNA levels in adipocytes compared with stromal-vascular cells from abdominal adipose tissue. Northern blot analysis (Fig. 4AGo) for PR, performed with total RNA after denaturing gel electrophoresis, demonstrated greater PR mRNA levels in adipose stromal cells compared with adipocytes. Slot-blot analysis (Fig. 4BGo) was performed to semiquantitate the difference in PR mRNA levels between the two cell fractions in five subjects. Northern blot analysis of ß-actin was used to control for differences in loading of total RNA. Densitometry values for the slots were expressed as the ratio of the value for the PR and the corresponding value for ß-actin. Stromal-vascular cells contained approximately 2.5-fold greater levels of PR mRNA compared with adipocytes.



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  		Figure 4. A, Northern blot analysis comparison of PR mRNA levels in adipocytes vs. stromal-vascular cells. Five micrograms total RNA was separated by denaturing gel electrophoresis, applied to nylon, and probed with a randomly primed labeled hPR cDNA. Insert, 28S and 18S ribosomal RNA bands of ethidium bromide gel. B, Slot-blot analysis was used to semiquantitate PR mRNA levels in adipocytes (Adip) vs. stromal-vascular (SV) cells of samples from five subjects. Five micrograms total RNA was applied to nylon and probed with a randomly primed labeled hPR cDNA. The membrane was then stripped and reprobed with a labeled ß-actin cDNA. Slot-blots were quantitated with laser densitometry, and results expressed as ratio of PR to ß-actin. For each subject, samples were run in triplicate, with SD bars showing variance. A paired t test for all patients showed a significant difference between SV and Adip, (P <= 0.001). A representative slot-blot is shown.

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
A substantial amount of clinical evidence indicates that sex steroids may play a role in fat tissue regulation and distribution. Prepubertal boys and girls do not differ significantly in adipose tissue percentage or distribution. However, with puberty, females experience an increase in fat percentage as well as selective adipose tissue deposition in the breast and gluteo-femoral regions. This gynoid fat distribution commonly exists until menopause in normal nonobese women. Women with disorders of androgen excess often display an upper body or android type of fat distribution characterized by abdominal adipose deposition and a higher waist-to-hip ratio (2). During menopause, at which time ovarian production of estrogen and progesterone ceases, the female phenotype becomes more android (11, 12). Because upper body fat distribution is strongly correlated with pathophysiology (13), the understanding of sex steroid regulation of adipose tissue distribution may be important in ultimately preventing this process and decreasing disease risk.

Detection of sex steroid receptors has been technically difficult in human adipose tissue because of the inherent properties of the tissue. In past studies, ERs could not be demonstrated with routine binding assays because of the high nonspecific binding of estrogens stored in adipose tissue (14). With the development of more sensitive assays, ER mRNA (by PCR and Northern blot analysis) and ER protein (8, 9) have been demonstrated in human adipose tissue. To date, there have been no reports of the presence of PR mRNA or protein (7, 15) in human adipose tissue, although specific progestin binding has been demonstrated in the adipose tissue of rat (16) and sheep (17). In addition to traditional target tissues, PR has been identified in such nonclassical human tissues as osteoclasts (18), the peripheral veins (19), and prostate stromal cells (20).

In this study, we were able to demonstrate PR mRNA by Northern blot analysis and PR protein by Western blot analysis in the abdominal subcutaneous adipose tissue of premenopausal women. Discrete transcripts of sizes identical to those present in uterine tissue can be detected in Northern blot analyses of total RNA isolated from human adipose tissue, suggesting that regulation of transcription for PR is as complicated in adipose tissue as in reproductive tissues (21). These multiple transcripts are obtained from two promoters, yielding hPR-A- and hPR-B- specific transcripts (22, 23), the identities of which have not been determined.

The physiological response to progesterone is conveyed by two discrete forms of the PR (hPR-A and hPR-B) in target tissues (24). The B isoform is a 933-amino acid protein that acts primarily as an activator of transcription. hPR-A (768 amino acids) is an N-terminally truncated form of the larger B protein lacking the first 164 amino acids and functions as a repressor of hPR-B activity (25). In addition, hPR-A can repress transcriptional activation of glucocorticoid, mineralocorticoid, and ERs, suggesting that PR may play a pivotal role in the regulation of other steroid hormones (26, 27).

Both the A and B isoforms of the PR appear to be present in human adipose tissue. The B isoform was of similar size to that of uterine tissue at approximately 116 kDa. The A isoform in adipose tissue was slightly greater in size (92 kDa) than the predominant A isoform in uterine tissue used in this study as a positive control (83 kDa). This may be because of differences in the degree of phosphorylation of the protein, which has been described in other tissues (28). The ratio of the two PR isoforms has been shown to vary in chick oviduct tissue according to estrogen status (29). Whether the ratio of the isoforms will vary in adipose tissue with changes in endogenous estrogen levels remains to be investigated.

Further analysis of the PR involved quantitation of the protein levels by a multiple antibody ELISA. The values of the PR in human abdominal adipose tissue of premenopausal women are similar to those reported by Watson et al. (14) in sheep and are much lower than the uterine control, as expected.

Differences in the cellular content of PR in human adipose tissue are also evident. In this study, we demonstrated higher levels of PR mRNA in the stromal-vascular cells compared with adipocytes. Previous studies have shown ER mRNA levels to be higher in adipocytes compared with stromal-vascular cells (8). In addition, cytochrome P450 aromatase, the enzyme responsible for conversion of C19 steroids into C18 estrogens, has higher activity and mRNA levels in stromal-vascular cells compared with adipocytes (8, 30). These observations suggest a differential type of regulation by sex steroids of the cells in human adipose tissue. Estrogen of ovarian origin or estrogen produced by aromatization in adipose stromal cells may transcriptionally regulate adipocytes. In contrast, progesterone of ovarian origin may primarily regulate adipose stromal cells. This selective distribution of ER and PR levels in different cells of a given tissue has also been reported with endometrium of the rabbit uterus (31), where PR levels are higher in endometrial stromal cells compared with glandular cells, but ER levels are higher in glandular cells.

Now that the presence of the ER and PR in human adipose tissue has been established, further studies will be possible to investigate the target genes for these sex steroids in this tissue. Ultimately, these studies will help clarify the role of sex steroids in the regulation and distribution of adipose tissue.


   Acknowledgments
 
We thank Dr. Geoffrey Greene for his kind gift of human PR cDNA. We gratefully acknowledge the technical assistance of Stephanie Weathers (Greenville Hospital System/Clemson University Biomedical Cooperative) and Dawn Blackhurst (Greenville Hospital System, Department of Medical Research).

Received June 2, 1997.

Revised October 17, 1997.

Accepted October 28, 1997.


   References
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 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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