High-Affinity Binding of Progesterone to the Plasma Membrane of Xenopus Oocytes: Characteristics of Binding and Hormonal and Developmental Control1

Liu, Zhiming; Patiño, Reynaldo

doi:10.1095/biolreprod49.5.980

Cited by 79 publications

(49 citation statements)

References 38 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Very little is currently understood about the early progesterone-induced signaling events, including the identity of the putative membrane progesterone binding protein. Previous work reported the presence of specific high affinity progesterone binding sites on Xenopus membranes (24,25). Our results confirm these reports, demonstrating high affinity progesterone binding sites (K d ϭ 3 nM) on Stage V-VI oocyte membranes but not on Stage I-III oocyte membranes FIG.…”

Section: Discussionsupporting

confidence: 92%

“…Oocyte Membrane Preparation-Oocyte membranes were prepared from Stage V-VI or Stage I-IIII oocytes as described (25). In summary, oocytes were homogenized with a Dounce homogenizer (Kontes, pestle A, 15 strokes) in membrane buffer (83 mM NaCl, 1 mM MgCl 2 , 1 mM phenylmethylsulfonyl fluoride, 10 mM Hepes, pH 7.6) at 4°C.…”

Section: Methodsmentioning

confidence: 99%

“…Third, progesterone injection directly into oocytes does not induce maturation (16,21,23). Finally, progesterone appears to bind specifically and with relatively high affinity to oocyte membranes (24,25). At this point, however, no progesterone binding proteins have been identified in Xenopus oocyte membranes.…”

mentioning

confidence: 97%

See 2 more Smart Citations

G Protein βγ Subunits Inhibit Nongenomic Progesterone-induced Signaling and Maturation in Xenopus laevis Oocytes

Lutz

Kim

Jahani

et al. 2000

Journal of Biological Chemistry

View full text Add to dashboard Cite

Progesterone-induced maturation of Xenopus oocytes is a well known example of nongenomic signaling by steroids; however, little is known about the early signaling events involved in this process. Previous work has suggested that G proteins and G protein-coupled receptors may be involved in progesterone-mediated oocyte maturation as well as in other nongenomic steroid-induced signaling events. To investigate the role of G proteins in nongenomic signaling by progesterone, the effects of modulating G␣ and G␤␥ levels in Xenopus oocytes on progesterone-induced signaling and maturation were examined. Our results demonstrate that G␤␥ subunits, rather than G␣, are the principal mediators of progesterone action in this system. We show that overexpression of G␤␥ inhibits both progesterone-induced maturation and activation of the MAPK pathway, whereas sequestration of endogenous G␤␥ subunits enhances progesterone-mediated signaling and maturation. These data are consistent with a model whereby endogenous free Xenopus G␤␥ subunits constitutively inhibit oocyte maturation. Progesterone may induce maturation by antagonizing this inhibition and therefore allowing cell cycle progression to occur. These studies offer new insight into the early signaling events mediated by progesterone and may be useful in characterizing and identifying the membrane progesterone receptor in oocytes.Steroid hormones are traditionally known to mediate their signaling and subsequent biological activities via nuclear receptors (1). Interestingly, many steroid-induced signaling events appear to be triggered independently from the classic nuclear receptor pathways. In fact, these processes likely involve steroid signaling via membrane receptors (2). Examples of rapid, nongenomic signaling by steroids are myriad, including aldosterone-induced increases in intracellular calcium in vascular smooth muscle cells (3-8), estrogen-mediated induction of nitric-oxide synthase in vascular endothelial cells (9 -12), vitamin D-induced increases in intracellular calcium in osteosarcoma cells (13)(14)(15), and progesterone-mediated maturation of amphibian and fish oocytes (16 -18).The phenomenon of progesterone-induced maturation of Xenopus oocytes serves as a useful experimental model for studying nongenomic steroid signaling (16, 19 -21). The maturation of an oocyte refers to the meiotic stage at which an oocyte rests. "Immature" oocytes are arrested in prophase of meiosis I. Before ovulation, oocytes are induced to re-enter the cell cycle, finally resting in metaphase II. These "mature" oocytes are then competent for ovulation and subsequent fertilization, after which the final stages of meiosis are completed (16).Evidence suggests that progesterone-induced maturation of Xenopus oocytes is mediated by cell surface rather than nuclear receptors. First, maturation is unaffected by the transcriptional inhibitor actinomycin D (21). Second, progesterone covalently attached to either polymers or bovine serum albumin and therefore unable to diffuse through the oocyte mem...

show abstract

Section: Discussionsupporting

confidence: 92%

Section: Methodsmentioning

confidence: 99%

See 1 more Smart Citation

G Protein βγ Subunits Inhibit Nongenomic Progesterone-induced Signaling and Maturation in Xenopus laevis Oocytes

Lutz

Kim

Jahani

et al. 2000

Journal of Biological Chemistry

View full text Add to dashboard Cite

show abstract

“…Whilst some of these rapid steroid effects are clearly mediated in some tissues by modulation of other receptors by progesterone or its metabolites (Baulieu & Robel 1995, Picard 1998, evidence has accumulated recently for the existence of non-genomic cell surface membrane steroid receptors for vitamin D, thyroid hormones, corticoids and the major sex steroids , Rupprecht et al 1996, Wehling 1997, Revelli et al 1998. In particular, membrane receptors for progesterone have been described in several tissues, including brain (Caldwell et al 1995, Joels 1997, Wiebe 1997, intestinal smooth muscle (Bielefeldt et al 1996), adrenal chromaffin cells (Dar & Zinder 1997), liver (Meyer et al , 1998, amphibian oocytes (Sadler & Maller 1982, Liu & Patino 1993, Bandyopadhyay et al 1998) and human sperm (Blackmore et al 1990, 1994, Alexander et al 1996, Ambhaikar & Puri 1998, Luconi et al 1998, where its presence may indicate fertilizing outcome ( Jacob et al 1998). Work on the human sperm membrane progesterone receptor has shown progesterone mediates a number of physiologically important events (Tesarik et al 1993, Aitken et al 1998, including stimulation of the acrosome reaction (Sabeur et al 1996) and hyperactivated sperm movement (Parinaud & Milhet 1996).…”

Section: Introductionmentioning

confidence: 99%

Bovine ovarian non-genomic progesterone binding sites: presence in follicular and luteal cell membranes

Rae

Menzies²,

Bramley³

1998

Journal of Endocrinology

View full text Add to dashboard Cite

We have shown recently that the bovine corpus luteum (CL) possesses specific luteal cell surface membrane binding sites for progesterone. We have now confirmed and extended these observations to compare the subcellular distribution of these binding sites in developing, mature and regressing CL. The median buoyant densities of luteal progesterone binding sites from early-, mid-and late-luteal phase CL were similar (though three of five density profiles for late-luteal phase CL showed association of steroid binding with a fraction with a lower density), and clearly resolved from nuclear, mitochondrial, lysosomal, peroxisomal, Golgi-endoplasmic reticulum-lysosomal and smooth endoplasmic reticulum markers. Specific binding of [3 H]progesterone overlapped with the distributions of 5 -nucleotidase and luteinizing hormone receptor (luteal cell surface membrane markers) in both control and digitonin-treated gradients at all stages of the luteal phase.Since steroidogenic 'large luteal' and 'small luteal' cells of the CL are derived from the granulosa cells (GC) and theca of the preovulatory follicle, we also investigated whether similar receptors were present in the follicle, and describe for the first time specific membrane binding sites for progesterone in purified GC and thecal membranes from healthy bovine follicles of different sizes. Specific binding increased linearly with GC and thecal membrane protein concentration; however, it was detectable only when digitonin was included in the binding incubation. Binding sites were specific for progesterone; unlabelled progesterone competed for [ 3 H]progesterone binding at low concentrations (IC 50 , 35 and 31 nmol/l) compared with testosterone (IC 50 , 905 and 870 nmol/l) and 4 -androstenedione (IC 50 , 1050 and 660 nmol/l) for GC and thecal receptors respectively. In contrast, oestradiol, oestrone, pregnenolone, cortisol, cholesterol, and a genomic progesterone receptor antagonist, RU486, competed poorly.Steroid binding was present in GC and thecal membranes of follicles of all sizes, but [ 3 H]progesterone binding to GC membranes decreased significantly with increasing follicle size (P<0·02), perhaps indicating developmental regulation of GC membrane non-genomic progesterone receptors in the preovulatory bovine follicle. We suggest that these membrane steroid receptors may be involved in the autocrine/paracrine regulation of follicular function by progesterone.

show abstract

“…Second, direct injection of steroids into oocytes does not appear to promote maturation (21). Third, specific highaffinity steroid binding sites (K d values in the 10-100 nM range) have been described in oocyte membrane preparations (16,(22)(23)(24). Unfortunately, these studies all have significant flaws: (i) BSA-conjugated steroid preparations have been shown to be ''leaky,'' with significant dissociation of steroid from the protein during the time required for oocyte maturation (25).…”

mentioning

confidence: 99%

The further redefining of steroid-mediated signaling

Hammes

2003

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

High-Affinity Binding of Progesterone to the Plasma Membrane of Xenopus Oocytes: Characteristics of Binding and Hormonal and Developmental Control1

Cited by 79 publications

References 38 publications

G Protein βγ Subunits Inhibit Nongenomic Progesterone-induced Signaling and Maturation in Xenopus laevis Oocytes

G Protein βγ Subunits Inhibit Nongenomic Progesterone-induced Signaling and Maturation in Xenopus laevis Oocytes

Bovine ovarian non-genomic progesterone binding sites: presence in follicular and luteal cell membranes

The further redefining of steroid-mediated signaling

Contact Info

Product

Resources

About