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In Situ Hybridization of High Density Lipoprotein (Scavenger, Type 1) Receptor Messenger Ribonucleic Acid (mRNA) during Folliculogenesis and Luteinization: Evidence for mRNA Expression and Induction by Human Chorionic Gonadotropin Specifically in Cell Types that Use Cholesterol for Steroidogenesis¹

Departments of Obstetrics and Gynecology and Biological Chemistry, University of Michigan Medical School, Ann Arbor, Michigan 48109

Address all correspondence and requests for reprints to: Dr. K. M. J. Menon, University of Michigan, 6428 Medical Science Building I, 1301 East Catherine Street, Ann Arbor, Michigan 48109-0617.

	Abstract

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The present studies were undertaken to examine the expression of the high density lipoprotein (HDL) receptor, SR-B1 messenger RNA (mRNA) in ovarian cell types during folliculogenesis and luteinization using in situ hybridization histochemistry and to examine its hormonal regulation using Northern blots. For the in situ study for HDL receptor mRNA localization, 21-day-old rats were treated with 50 IU PMSG, and ovaries were collected 0, 24, and 56 h postinjection. At 56 h, animals were treated with a single dose of hCG, and ovaries were subsequently collected at 6-, 12-, 24-, and 72-h and 5-day intervals. In addition, on day 4 of pseudopregnancy, a second dose of 50 IU hCG or saline was administered, and ovaries were collected at 12, 24, and 48 h to determine the induction of the expression of HDL receptor mRNA. The results of in situ hybridization histochemistry showed that in the immature ovary, HDL receptor mRNA is associated with theca interna and interstitial cells (stroma). The mRNA expression in these cell types increased with PMSG treatment, but no signal was detected in the granulosa cells. Northern blot analysis also showed a marked increase in mRNA content in thecal and interstitial cells during follicular development. During luteinization, the intensity of the signal began to appear in the luteinized granulosa cells. With the completion of luteinization, the signal in the corpus luteum tissue became more intense. Further treatment with hCG increased the HDL receptor mRNA content compared with that in the saline-treated control. These results demonstrate that the cholesterol-using cell types of the ovary, namely the interstitial cells, thecal cells, and fully luteinized granulosa cells are endowed with the HDL receptor mRNA, which provides credence to the functional significance of the role of HDL receptor SR-B1 in cholesterol transport and ovarian steroidogenesis.

	Introduction

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PLASMA lipoproteins are the major source of cholesterol for steroidogenesis by the rat ovarian tissues (1, 2). The uptake of low density lipoprotein (LDL)-derived cholesterol involves specific binding of the LDL particles to cell surface receptors followed by internalization of the LDL particles and lysosomal hydrolysis to release cholesterol esters, as described by Brown and Goldstein (3). However, utilization of the high density lipoprotein (HDL)-derived cholesterol is not understood to the same degree as is utilization of LDL cholesterol. Receptors for LDL and HDL have been characterized in the membrane fractions obtained from ovarian tissues (4, 5, 6, 7, 8). Specific binding of HDL fractions to high affinity receptors has been demonstrated in other systems as well (9, 10). Two reports have appeared in the literature that describe the cloning of putative HDL receptors (11, 12). Recently, it has been suggested that the scavenger receptor class B type 1, SR-B1, a previously identified protein that specifically recognizes acetylated LDL particles, is capable of recognizing HDL particles and therefore functions as the HDL receptor (13, 14, 15). The scavenger receptor SR-B1 was expression cloned from a Chinese hamster ovary (CHO) cell variant and was shown to be a member of CD36 family of membrane proteins (13). Like CD36, the scavenger receptor SR-B1 exhibits high affinity binding for acetylated LDL (13).

Previous studies from our laboratory have established the presence of a scavenger receptor in the rat luteal cells that specifically binds acetylated LDL with high affinity and have shown that this receptor is distinct from the LDL receptor (16). Additionally, we showed that the rat luteal cells use acetylated LDL for progesterone production (16). Although acetylated LDL was capable of supplying cholesterol for steroid synthesis in the luteal tissue, its physiological significance was not understood, as acetylated LDL is not a naturally occurring ligand. As it appears that the scavenger receptor SR-B1 might be the HDL receptor, the present studies were undertaken to examine its physiological role in ovarian tissue during follicular development and corpus luteum formation. Specifically, we have examined the expression of SR-B1 messenger RNA (mRNA) in ovarian tissue using in situ hybridization histochemistry. Our results show that SR-B1 mRNA is expressed in steroidogenic ovarian cells in a manner consistent with their use of exogenous cholesterol for steroid hormone production.

	Materials and Methods

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Animals
Immature 21-day-old Sprague-Dawley female rats (Harlan Farms, Indianapolis, IN) were injected sc with 50 IU PMSG (Calbiochem, La Jolla, CA), followed by 25 IU hCG (supplied by the Center for Population Research, NIH, and NIAMDD) 56 h later to induce superovulation and subsequent luteinization (17). When indicated, pseudopregnant animals were treated with 50 IU hCG on day 4 of pseudopregnancy; control rats received an equal volume of saline. Ovaries were collected at specific time periods, frozen in liquid nitrogen, and stored until use at -80 C.

In situ hybridization
Ovaries frozen in OCT compound (Miles, Elkhart, IN) were cut at -20 C using a Reichert 2800 Frigocut-N cryostat (Leica, Deerfield, IL), and 10-µm sections were mounted on silane-coated slides. Tissue sections were fixed in 4% paraformaldehyde (pH 7.4) for 1 h, washed in PBS for 15 min, incubated with proteinase K (1 µg/ml) for 10 min at 37 C, and rinsed with distilled deionized water. Subsequently, slides were placed in 0.1 M triethanolamine (pH 8.0), and after the addition of acetic anhydride (final concentration, 0.25%, vol/vol), they were incubated for 10 min. Sections were then washed with 2 x SSC (SSC = 0.15 M NaCl and 0.015 M sodium citrate), dehydrated in graded alcohols (50–100%), and dried. Antisense and sense [³⁵S]UTP-labeled RNA probes were synthesized from 308-bp SR-B1 complementary DNA (cDNA; provided by Dr. Monte Krieger, Massachusetts Institute of Technology, Cambridge, MA) in pBluescript SK⁺ vector using T3 and T7 polymerase (18). The SR-B1 probe was amplified from the SR-B1 cDNA sequence corresponding to nucleotides 170–477 by PCR cloning (14). The RNA probe [1–3 x 10⁷ cpm/ml in hybridization buffer (75% formamide, 3 x SSC, 1 x Denhardt’s reagent [0.02% BSA, 0.02% Ficoll, and 0.02% polyvinylpyrrolidone], 0.05 M sodium phosphate (pH 7.4), 10% dextran sulfate, 1 mM dithiothreitol, and 200 µg/ml yeast transfer RNA)] was applied to the tissue sections, coverslips were overlaid and sealed with rubber cement, and slides were incubated at 55 C overnight in a moist chamber, as previously described (19). After hybridization, sections were washed in 2 x SSC, treated with ribonuclease A (200 µg/ml) and ribonuclease T1 (4 U/ml) at 37 C for 1 h, and washed in increasingly lower concentrations of SSC (2 to 0.2 x). After a final incubation in 0.1 x SSC-0.1% SDS for 1 h at 55 C, sections were dehydrated through graded alcohols (50–100%) and dried. The slides were processed for liquid emulsion autoradiography using NTB-2 emulsion (Eastman Kodak, Rochester, NY). Slides were developed after 2–5 days and counterstained with hematoxylin-eosin.

Northern analysis
Total RNA was extracted from tissues using the procedures of Chomczynski and Sacchi (20). Tissues were homogenized in a solution of guanidine isothiocyanate, acidified with 2 M sodium acetate (pH 4.0), and extracted with water-saturated phenol and chloroform-isoamyl alcohol (49:1). RNA remaining in the aqueous phase was precipitated overnight at 20 C using 3 vol ethanol. RNA was spectrophotometrically quantified, and its purity was determined by the A₂₆₀/A₂₈₀ ratio. Aliquots of total RNA were separated by electrophoresis in 1.2% agarose-formaldehyde gels and transferred to nitrocellulose membranes using 10 x SSC. Blots were UV cross-linked and prehybridized at 42 C for 2 h in a solution containing salmon sperm DNA (0.5 mg/ml) and 2 x hybridization buffer [1.5 NaCl and 0.1 TES (N-Tris[hydroxy-methyl]-methyl-2-aminoethanesulfonic acid, pH 7.1; 0.1 M EDTA; and 2 x Denhardt’s solution] diluted 1:1 with deionized formamide. An SR-B1 cDNA probe (308 bp) was radiolabeled using [-³²P]deoxy-CTP (ICN, Irvine, CA) and the Klenow fragment of DNA polymerase, and hybridized to blots overnight at 42 C in fresh hybridization buffer using 2 x 10⁷ cpm labeled probe. Hybridized blots were washed four times with 2 x SSC containing 0.1% SDS for 10 min each time at room temperature and once at 60 C for 30 min. The washed blots were exposed overnight at -70 C to Kodak XAR film in a cassette containing intensifying screens. The film was developed, and the signals were measured using a Zeineh (Fullerton, CA) soft laser scanning densitometer (model SL-TRFF). After stripping the blots, they were rehybridized to a cDNA probe corresponding to 18S ribosomal RNA radiolabeled with [-³²P]deoxy CTP as described above to normalize for RNA in the Northern blots.

	Results

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SR-B1 expression during follicular development
The expression of SR-B1 mRNA during rat ovarian follicular development is shown in Fig. 1. Twenty-one-day-old rats were treated with 50 IU PMSG, and the ovaries were collected at 0, 28, and 56 h of treatment. RNA was extracted, and Northern blots were performed using 308 bp SR-B1 cDNA probe. The blots of the SR-B1 mRNA and the hybridization signal of the 18S RNA are shown in Fig. 1A. The densitometric scans of the SR-B1 mRNA normalized for the 18S RNA are shown in Fig. 1B. The results show that there was an approximately 3-fold increase in the expression of SR-B1 mRNA from 0 to 56 h.

View larger version (37K): [in this window] [in a new window]   Figure 1. SR-B1 mRNA levels during follicular development. Total RNA was extracted from ovaries collected 0, 28, and 56 h after PMSG injection, and Northern blot analysis was performed using radiolabeled SR-B1 cDNA probe (A). Radiolabeled cDNA for 18S ribosomal RNA was used to monitor loading. Densitometric units corresponding to SR-B1 mRNA are expressed relative to the 18S ribosomal RNA signal at each time interval (B). The results presented are representative of one of three experiments.

View larger version (166K): [in this window] [in a new window]   Figure 2. In situ hybridization of SR-B1 mRNA during follicular development: 0 h. Ovaries were collected from immature (21-day-old) rats. Tissue sections were hybridized with antisense SR-B1 probe and photographed at x15 magnification using darkfield optics to show hybridization (A) and brightfield optics to show structures (B).

View larger version (167K): [in this window] [in a new window]   Figure 3. In situ hybridization of SR-B1 mRNA during follicular development: 24 h. Immature rats were injected with 50 IU PMSG, and ovaries were collected 24 h postinjection. A represents photomicrographs of ovarian sections hybridized with antisense SR-B1 probe using darkfield optics, and B represents brightfield photomicrographs.

View larger version (156K): [in this window] [in a new window]   Figure 4. In situ hybridization of SR-B1 mRNA during follicular development: 56 h. Ovaries were collected 56 h after PMSG treatment. A, Darkfield photomicrography; B, brightfield photomicrography.

The darkfield photomicrograph of the in situ hybridization of the ³⁵S-labeled antisense SR-B1 RNA 6 h after hCG administration is shown in Fig. 5A, and the corresponding brightfield photomicrograph is shown in Fig. 5B. The intensity of hybridization to the thecal cells was further increased, but the hybridization to granulosa cells was only beginning to develop, as luteinization of the granulosa cells was only minimal at this time. At 12 h, the hybridization signal in the granulosa cells was not markedly increased. The hybridization signal was also detectable in follicles that were not fully developed; surrounding layers of theca also responded to hCG treatment (Fig. 6, A and B). As the corpus luteum was fully developed, the luteinized granulosa cells showed significant hybridization signal as shown in Fig. 7. By 72 h, the predominant cell types, which showed high intensity hybridization signal, were primarily the luteal cells in corpora lutea, with significantly less hybridizable SR-B1 mRNA in the other existing ovarian structures, such as regressing follicles and stromal cells (Fig. 8, A and B). By day 5, the hybridization signal showed dramatic increases (Fig. 9A) in the corpora lutea. At this time, the ovary exhibited the presence of a number of well developed corpora lutea (Fig. 9B). Thus, the expression of SR-B1 shows good correlation with the steroidogenic potential of the corpora lutea. No appreciable hybridization signal was detected when the tissue sections (120 h after hCG treatment) were hybridized with a 308-bp SR-B1 sense RNA, showing the specificity of the hybridization reaction (Fig. 10).

View larger version (157K): [in this window] [in a new window]   Figure 5. In situ hybridization of SR-B1 mRNA during luteinization. Ovaries were isolated from PMSG-primed rats 6 h after hCG injection. Tissue sections were hybridized with antisense SR-B1 probe and photographed at x15 magnification using darkfield (A) or brightfield (B) optics.

View larger version (141K): [in this window] [in a new window]   Figure 6. In situ hybridization of SR-B1 mRNA expression 12 h after treatment with hCG. A, Darkfield photomicrographs; B, brightfield photomicrographs.

View larger version (145K): [in this window] [in a new window]   Figure 7. In situ hybridization of SR-B1 mRNA expression 24 h after hCG administration. A, Darkfield photomicrographs; B, brightfield photomicrographs.

View larger version (157K): [in this window] [in a new window]   Figure 8. In situ hybridization of SR-B1 expression 72 h after hCG injection. A, Darkfield photomicrographs; B, brightfield photomicrographs.

View larger version (141K): [in this window] [in a new window]   Figure 9. In situ hybridization of SR-B1 expression 120 h after hCG injection. A, Darkfield photomicrographs; B, brightfield photomicrographs.

View larger version (120K): [in this window] [in a new window]   Figure 10. In situ hybridization of sections of ovaries (120 h after hCG injection) hybridized with the 308-bp SR-B1 sense RNA probe.

View larger version (36K): [in this window] [in a new window]   Figure 11. hCG induction of SR-B1 mRNA. Rats were injected with saline (control) or 50 IU hCG on day 4 of pseudopregnancy. At the time points indicated, total RNA was processed for Northern blot analysis using radiolabeled SR-B1 cDNA probe (A). Radiolabeled cDNA for 18S ribosomal RNA was used to monitor loading. SR-B1 mRNA densitometric units obtained from autoradiogram were normalized for 18S ribosomal RNA (B). The data presented are representative of experiments performed three times.

	Discussion

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To determine whether SR-B1 is expressed in cell types that use HDL-derived cholesterol for steroidogenesis, we used in situ hybridization histochemistry to identify SR-B1 mRNA expression in various ovarian cell types during folliculogenesis, corpus luteum formation, and the life span of the corpus luteum. The ovary is a dynamic structure and undergoes marked changes during the reproductive cycle (23). During the early phase of follicle maturation, the major steroidogenic cell types are the interstitial and thecal cells, both of which convert cholesterol to steroid hormones. The principal secretory products at this stage of the ovarian cycle are the androgens (24). The granulosa cells become active in steroid synthesis during follicle maturation; these cells convert androgens produced by the theca-interstitial cells to estrogens (25). After ovulation, the granulosa cells undergo differentiation, resulting in the formation of luteal cells, which have the ability to convert cholesterol to steroid hormones. Thus, if SR-B1 is physiologically significant in cholesterol transport into the ovary for steroid hormone biosynthesis, it is expected that its expression will be detectable in cell types that use cholesterol for steroid production.

Our results show that the SR-B1 is minimally expressed at the onset of follicle development. At this stage, the ovary contains numerous primordial follicles and interstitial cells and layers of thecal cells. The major steroidogenic products at this stage of follicular growth are progesterone, androst-4-ene-3,17-dione, testosterone, and their metabolites (24). It is interesting to note that the SR-B1 expression at this stage is associated with thecal and interstitial cells, with no signal detected in the granulosa cells. Dramatic changes in SR-B1 expression were seen during follicle maturation induced by PMSG administration. During this period, examination of SR-B1 mRNA expression revealed that the intensity of the signal significantly increased in layers of thecal cells surrounding the follicles. No expression of SR-B1 mRNA was detected in the granulosa cells even after PMSG administration. It is interesting to note that SR-B1 is localized exclusively in thecal and interstitial cells, cell types using cholesterol for conversion to steroids. The absence of the hybridization signal in the granulosa cells is not surprising because the major steroidogenic function of the granulosa cells is to convert androgens to estrogens. The source of cholesterol needed for other functions, such as cell membrane biogenesis, in the granulosa cells is not understood.

As luteinization proceeds, a dramatic shift in the cellular localization of SR-B1 mRNA became apparent. The luteinized granulosa cells showed abundant expression of SR-B1 mRNA, as evidenced by the increased intensity of the hybridization signal in the corpus luteum. As the corpora lutea were fully developed after hCG injection, only a few follicles were present in the ovary, and they showed no evidence of the SR-B1 expression. The luteal cells showed bright in situ hybridization signals. As we have shown previously that the binding of acetylated LDL, a ligand for SR-B1, was induced in the luteal cell membrane by the administration of hCG, the possible effect of hormone treatment on the expression of SR-B1 mRNA was examined. Examination of the Northern blots of SR-B1 mRNA revealed that hCG administration increased the expression of SR-B1 mRNA. This is consistent with our previous studies in which we have demonstrated the induction of ¹²⁵I-acetylated LDL binding to luteal cell membranes after hCG administration (16).

These results clearly show that SR-B1 mRNA is expressed in the thecal cells, corpora lutea, and interstitial cells, but not in the granulosa cells, before luteinization. It is interesting to note that the cells expressing SR-B1 are also capable of using cholesterol for steroid hormone biosynthesis. For example, conversion of cholesterol to pregnenolone takes place in all of these cell types, except granulosa cells, which acquire androstenedione and testosterone from the thecal cells which are then converted to estrogens. The relative abundance of SR-B1 mRNA in the thecal cells during folliculogenesis, its increase during the life span of the corpus luteum, and its inducibility by hCG further support the role of SR-B1 in ovarian physiology in a manner consistent with the steroidogenic activity of these cells requiring cholesterol. The mechanism of the interaction of SR-B1 protein present in the ovarian membranes with HDL particles and the mechanism of cholesterol uptake mediated by this protein from cholesterol-laden particles into the ovary require further investigation.

	Acknowledgments

 
The authors thank Dr. Monte Krieger for providing us with SR-B1 cDNA clone, and Kay Brabec for assistance with the preparation of tissue sections for in situ hybridization. hCG was supplied by the Center for Population Research, NICHHD, through the National Hormone and Pituitary Program.

	Footnotes

 
¹ This work was supported by NIH Grant HD-06656. This study used services provided by the Morphology Core Facility, which is supported by NIH Grant I-P30-HD-18258.

Received February 6, 1998.

	References

Top Abstract Introduction Materials and Methods Results Discussion References

 

1. Azhar S, Menon M, Menon KMJ 1981 Receptor-mediated gonadotropin action in the ovary. Demonstration of acute dependence of rat luteal cells on exogenously supplied steroid precursor (sterols) for gonadotropin-induced steroidogenesis. Biochim Biophys Acta 665:362–375[Medline]
2. Gwynne JT, Strauss III JF 1982 The role of lipoproteins in steroidogenesis and cholesterol metabolism in steroidogenic glands. Endocr Rev 3:299–329[Medline]
3. Brown MS, Goldstein JL 1986 The low-density lipoprotein pathway and its relation to atherosclerosis. Science 232:34–47[Free Full Text]
4. Hwang J, Menon KMJ 1983 Characterization of low density and high density lipoprotein receptors in the rat corpus luteum and regulation by gonadotropin. J Biol Chem 258:8020–8027[Abstract/Free Full Text]
5. Hwang J, Menon KMJ 1985 Binding of apolipoprotein A-I and A-II after recombination with phospholipid vesicles to the high density lipoprotein receptor of luteinized rat ovary. J Biol Chem 260:5660–5668[Abstract/Free Full Text]
6. Ferreri K, Menon KMJ 1990 Detection of a 58-kilodalton high density lipoprotein-binding protein in the membrane fraction of luteinized rat ovaries. Endocrinology 126:2137–2144[Abstract]
7. Ghosh KK, Menon KMJ 1987 Induction of high-density-lipoprotein receptors in rat corpus luteum by human choriogonadotropin. Biochem J 244:471–479[Medline]
8. Ferreri K, Menon KMJ 1992 Characterization and isolation of a high-density-lipoprotein-binding protein from bovine corpus luteum plasma membrane. Biochem J 287:841–848
9. Graham DL, Oram JF 1987 Identification and characterization of a high density lipoprotein-binding protein in cell membranes by ligand blotting. J Biol Chem 262:7439–7442[Abstract/Free Full Text]
10. Fidge NH 1986 Partial purification of a high-density lipoprotein-binding protein from rat liver and kidney membranes. FEBS Lett 199:265–268[CrossRef][Medline]
11. McKnight GL, Reasoner J, Gilbert T, Sundquist KO, Hokland B, McKernan PA, Champagne J, Johnson CJ, Bailey MD, Holly R, O’Hara PJ, Oram JF 1992 Cloning and expression of a cellular high-density lipoprotein-binding protein that is up-regulated by cholesterol loading of cells. J Biol Chem 276:12131–12141
12. Matsumoto A, Mitchell A, Kurata H, Pyle L, Kondo K, Itakura H, Fidge N 1997 Cloning and characterization of HB2, a candidate high density lipoprotein receptor. Sequence homology with members of the immunoglobulin superfamily of membrane proteins. J Biol Chem 272:16778–16782[Abstract/Free Full Text]
13. Acton S, Scherer P, Lodish H, Krieger M 1994 Expression cloning of SR-B1, a CD36-related Class B scavenger receptor. J Biol Chem 269:21003–21009[Abstract/Free Full Text]
14. Acton S, Rigotti A, Landschultz KT, Xu S, Hobbs HH, Krieger M 1996 Identification of scavenger receptor SR-B1 as a high density lipoprotein receptor. Science 271:518–520[Abstract]
15. Rigotti A, Trigatti B, Babitt J, Penman M, Xu S, Krieger M 1997 Scavenger receptor B1: a cell surface receptor for high density lipoprotein. Curr Opin Lipidol 8:181–188[CrossRef][Medline]
16. Chen Z, Menon KMJ 1993 Identification of a scavenger receptor in rat luteal cells which recognizes chemically modified lipoproteins and mediates the uptake of cholesterol for steroidogenesis. Biochim Biophys Acta 1150:79–88[Medline]
17. Parlow AF 1958 A rapid bioassay method for LH and factors stimulating LH secretion. Fed Proc 17:402
18. Sambrook EJ, Maniatis P 1989 Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, pp 1027–1037
19. Peegel H, Randolph JR, Midgley AR, Menon KMJ 1995 In situ hybridization of luteinizing hormone/human chorionic gonadotropin receptor messenger ribonucleic acid during hormone-induced down-regulation and the subsequent recovery in rat corpus luteum. Endocrinology 135:1044–1051[Abstract]
20. Chomczynski P, Sacchi N 1987 Single-step method of RNA isolation by acid guaninium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159[Medline]
21. Landschulz KT, Pathak RK, Rigotti A, Krieger M, Hobbs HH 1996 Regulation of scavenger receptor, class B, type I, a high density lipoprotein receptor, in liver and steroidogenic tissues of the rat. J Clin Invest 98:984–995[Medline]
22. Mizutani T, Sonoda Y, Mineqishi T, Wakobayashi K, Miyamoto T 1997 Cloning, characterization, and cellular distribution of rat scavenger receptor class B type 1 (SRB1) in the ovary. Biochem Biophys Res Commun 234:499–505[CrossRef][Medline]
23. Baker TG 1972 Oogenesis and Ovulation. In: Austin CR, Short RV (eds) Reproduction in Mammals, book 1. Cambridge University Press, Cambridge, pp 14–45
24. Magoffin DA, Erickson GF 1988 An improved method for primary culture of ovarian androgen-producing cells in serum-free medium: effect of lipoproteins, insulin and insulin-like growth factor-1. In Vitro Cell Dev Biol 24:862–864[Medline]
25. Bjersing L 1967 On the morphology and endocrine function of granulosa cells of ovarian follicles and corpora lutea. Acta Endocrinol [Suppl] (Copenh) 125:1–23

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				B. Trigatti, H. Rayburn, M. Vinals, A. Braun, H. Miettinen, M. Penman, M. Hertz, M. Schrenzel, L. Amigo, A. Rigotti, et al. Influence of the high density lipoprotein receptor SR-BI on reproductive and cardiovascular pathophysiology PNAS, August 3, 1999; 96(16): 9322 - 9327. [Abstract] [Full Text] [PDF]

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