Thrombospondin-1 Expression Is Increased during Follicular Atresia in the Primate Ovary

Thrombospondin (TSP)-1 is an antiangiogenic extracellular matrix glycoprotein that modulates several aspects of cellular function. The aim of this study was to determine the pattern of TSP-1 mRNA and protein expression as well as expression of its receptor CD36 in the marmoset ovary and to investigate the effects of inhibition of gonadotropins or VEGF activity on TSP-1 and CD36 expression in vivo. GnRH antagonist or VEGF Trap, a soluble decoy receptor, was administered on d 0 of the follicular phase of the cycle, and ovaries were collected at the end of the follicular phase (d 10). TSP-1 mRNA and protein were present in granulosa cells of preantral and antral follicles, with the highest staining at the late secondary and tertiary stages. Moreover, expression of TSP-1 mRNA and protein was significantly increased in tertiary follicles undergoing atresia. CD36 protein was detected in granulosa cells of preantral and antral follicles as well as in endothelial cells of large vessels. Inhibition of gonadotropin secretion or VEGF activity had no effect on TSP-1 expression; however, expression of CD36 protein was inhibited by the VEGF Trap. In conclusion, TSP-1 may be involved in the cessation of angiogenesis in follicles undergoing atresia; alternatively, TSP-1 may act on granulosa and/or endothelial cells to promote follicular atresia in the ovary. Angiogenesis is likely to involve a balance between pro- and antiangiogenic factors. Our results suggest that loss of VEGF activity does not regulate TSP-1 expression directly but may influence TSP-1 activity via down-regulation of the CD36 receptor.

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Expression of Anti-Mullerian Hormone Protein during Early Follicular Development in the Primate Ovary in Vivo Is Influenced by Suppression of Gonadotropin Secretion and Inhibition of Vascular Endothelial Growth Factor

Endocrinology ◽

10.1210/en.2006-1501 ◽

2007 ◽

Vol 148 (5) ◽

pp. 2273-2281 ◽

Cited By ~ 34

Author(s):

Fiona H. Thomas ◽

Evelyn E. Telfer ◽

Hamish M. Fraser

Keyword(s):

Gnrh Antagonist ◽

Follicular Development ◽

Follicular Phase ◽

Vascular Endothelial ◽

Gonadotropin Secretion ◽

Preantral Follicles ◽

Antral Follicles ◽

Endothelial Growth Factor ◽

Vegf Trap

Anti-Mullerian hormone (AMH) plays a role during early follicular development and selection. The aim of this study was to determine the pattern of AMH protein expression in the marmoset ovary and to investigate the effects of inhibition of gonadotropins or vascular endothelial growth factor (VEGF) activity on AMH expression in vivo. GnRH antagonist or VEGF Trap, a soluble decoy receptor, was administered on d 0 or 5 of the follicular phase of the cycle, and ovaries were collected at the end of the follicular phase (d 10). AMH protein was expressed in the marmoset ovary in granulosa cells from the primary stage, with the most abundant staining at the preantral and early antral stages. Inhibition of gonadotropin secretion or VEGF activity between d 0–10 of the cycle decreased AMH expression in early preantral follicles (P < 0.01), and AMH expression was decreased in late preantral follicles in the presence of the VEGF Trap (P < 0.01), compared with controls. There was significantly less AMH expression in early antral follicles with both treatments (P < 0.01), and a decrease in the ratio of oocyte-associated/basement-membrane-associated granulosa cell expression of AMH (P < 0.05). When treatments were administered from d 5–10 of the cycle, both VEGF Trap and GnRH antagonist decreased AMH expression in preantral follicles (P < 0.01) but had no significant effect on early antral follicles. In conclusion, VEGF and gonadotropins are involved in the regulation of expression of AMH in the marmoset. This AMH expression may be a marker of abnormal folliculogenesis in the absence of gonadotropin stimulation or functional angiogenesis.

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Identification of androgen receptor phosphorylation in the primate ovary in vivo

Reproduction ◽

10.1530/rep-10-0140 ◽

2010 ◽

Vol 140 (1) ◽

pp. 93-104 ◽

Cited By ~ 11

Author(s):

Iain J McEwan ◽

Dagmara McGuinness ◽

Colin W Hay ◽

Robert P Millar ◽

Philippa T K Saunders ◽

...

Keyword(s):

Endothelial Cells ◽

Androgen Receptor ◽

Granulosa Cells ◽

Gnrh Antagonist ◽

Follicular Phase ◽

Surface Epithelium ◽

Control Group ◽

Target Tissue ◽

Receptor Phosphorylation

The androgen receptor (AR) is a member of the nuclear receptor superfamily, and is important for both male and female reproductive health. The receptor is a target for a number of post-translational modifications including phosphorylation, which has been intensively studied in vitro. However, little is known about the phosphorylation status of the receptor in target tissues in vivo. The common marmoset is a useful model for studying human reproductive functions, and comparison of the AR primary sequence from this primate shows high conservation of serines known to be phosphorylated in the human receptor and corresponding flanking amino acids. We have used a panel of phosphospecific antibodies to study AR phosphorylation in the marmoset ovary throughout the follicular phase and after treatment with GNRH antagonist or testosterone propionate. In normal follicular phase ovaries, total AR (both phosphorylated and non-phosphorylated forms) immunopositive staining was observed in several cell types including granulosa cells of developing follicles, theca cells and endothelial cells lining blood vessels. Receptor phosphorylation at serines 81, 308, and 650 was detected primarily in the granulosa cells of developing follicles, surface epithelium, and vessel endothelial cells. Testosterone treatment lead to a modest increase in AR staining in all stages of follicle studied, while GNRH antagonist had no effect. Neither treatment significantly altered the pattern of phosphorylation compared to the control group. These results demonstrate that phosphorylation of the AR occurs, at a subset of serine residues, in a reproductive target tissue in vivo, which appears refractory to hormonal manipulations.

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Epidermal growth factor acts directly on the sheep ovary in vivo to inhibit oestradiol-17β and inhibin secretion and enhance progesterone secretion

Journal of Endocrinology ◽

10.1677/joe.0.1370253 ◽

1993 ◽

Vol 137 (2) ◽

pp. 253-264 ◽

Cited By ~ 18

Author(s):

J. F. Murray ◽

J. A. Downing ◽

G. Evans ◽

J. K. Findlay ◽

R. J. Scaramuzzi

Keyword(s):

Growth Factor ◽

Epidermal Growth Factor ◽

Granulosa Cells ◽

Ovarian Function ◽

Jugular Vein ◽

Follicular Phase ◽

Antral Follicles ◽

Progesterone Secretion ◽

Epidermal Growth

ABSTRACT Epidermal growth factor (EGF) is a potential intra-ovarian modulator of gonadotroph action on differentiated follicular cells. Specific binding sites have been identified in the ovary and functional differentiation in cultured granulosa cells can be modulated by treatment with EGF. The aim of this study was to determine if EGF was capable of altering ovarian function in vivo during the follicular phase of the sheep oestrous cycle. Fourteen cross-bred ewes with ovarian autotransplants were treated with progestagen pessaries for 12 days. Three ewes were infused with murine EGF (mEGF) via the jugular vein (75 μg/kg bodyweight per 12 h) during the 12 h preceding progestagen pessary withdrawal, and received an injection of a prostaglandin analogue at 0 h to induce luteolysis. Over the same time-period, two doses of EGF were administered to other groups of ewes by infusion into the ovarian artery (low: 6 μg/12 h, n = 3 and high: 60 μg/12 h, n = 3). The remaining five ewes were not infused with EGF (controls). Jugular and ovarian venous blood samples were taken at 10-min intervals at two stages during the follicular phase (21–27 h and 38–42 h after pessary withdrawal) and every 2 h from 44 to 76 or 86 h. mEGF, LH, FSH, inhibin, androstenedione, oestradiol-17β and progesterone concentrations in plasma were determined using radioimmunoassays. The secretion rates of androstenedione, oestradiol, progesterone and inhibin by the ovary were calculated. EGF acted directly on the ovary in a dose-dependent manner. Oestradiol secretion was inhibited following treatment with EGF but androstenedione secretion was unaffected. EGF appears therefore to act within the granulosa cells to inhibit aromatization. Inhibin secretion was also suppressed by treatment with EGF, though it was not possible to determine if this was caused by a direct or indirect action of EGF on granulosa cells. The rate of progesterone secretion increased in ewes receiving systemic (i.e. via the jugular vein) and high-dose intra-arterial infusions of EGF, even though a preovulatory LH surge was not observed in these animals during the entire experimental period. Concomitant increases in both LH and FSH secretion were associated with these effects of EGF on ovarian function. In conclusion, EGF appears to act directly on the granulosa cells of the follicle to inhibit aromatization and also to inhibit inhibin production. The low levels of oestradiol and inhibin in the presence of high levels of gonadotrophin indicate that atresia may have been induced in medium to large antral follicles. The increase in progesterone secretion following high doses of EGF may be derived from a luteinized follicle. FSH-stimulated functions cease when a follicle luteinizes and progesterone secretion commences. EGF treatment inhibited both oestradiol and inhibin secretion whilst enhancing progesterone which suggests that EGF may also be involved in the induction of functional luteinization. EGF or an EGF-like substance may therefore be an important factor in the induction of functional luteinization, with atresia occurring in antral follicles which are exposed to EGF too early in their development. Journal of Endocrinology (1993) 137, 253–264

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A Thrombospondin-Mimetic Peptide, ABT-898, Suppresses Angiogenesis and Promotes Follicular Atresia in Pre- and Early-Antral Follicles in Vivo

Endocrinology ◽

10.1210/en.2010-0283 ◽

2010 ◽

Vol 151 (12) ◽

pp. 5905-5915 ◽

Cited By ~ 33

Author(s):

Samantha A. Garside ◽

Jack Henkin ◽

Keith D. Morris ◽

Suzanne M. Norvell ◽

Fiona H. Thomas ◽

...

Keyword(s):

Granulosa Cells ◽

Polycystic Ovary ◽

Follicular Phase ◽

Vascular Endothelial ◽

Ovulatory Cycle ◽

Antral Follicles ◽

Angiogenesis Assay ◽

Endothelial Growth Factor

Using a novel in vitro angiogenesis assay, we previously showed that thrombospondin (TSP)-1 has antiangiogenic effects on rat follicles and induces apoptosis in granulosa cells in vitro. ABT-898 is an octapeptide mimetic of TSP-1 closely related to ABT-510. Here, we demonstrate the inhibitory effects of ABT-898 on follicular angiogenesis and its proapoptotic effect on granulosa cells. To investigate the potential of this peptide to inhibit follicular angiogenesis in vivo, marmoset monkeys were treated with 2.5 mg/kg ABT-898 twice daily throughout the follicular phase of the cycle. Although treatment did not block emergence of dominant follicles, angiogenesis was reduced in preantral and early-antral follicles. Furthermore, the incidence of atresia at these follicle stages was increased. To investigate whether treatment with ABT-898 would interfere with the timing or duration of the normal ovulatory rise in plasma progesterone, marmosets were treated with a depot formulation containing 25 mg ABT-898 at the start of the follicular phase, with a second injection after 2 wk. Despite active concentrations of peptide being maintained in the circulation, no apparent effects on the ovulatory cycle were observed. Taken together, these results indicate that ABT-898 is capable of having a dual effect by inhibiting follicular angiogenesis and promoting atresia of antral follicles in vivo but does not prevent ovulation or induce luteolysis, as has been observed with direct vascular endothelial growth factor inhibitors. These results suggest that ABT-898 could be a novel therapeutic to inhibit abnormal angiogenesis and induce atresia of accumulated follicles in polycystic ovary syndrome.

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Genome wide effects of oleic acid on cultured bovine granulosa cells: evidence for the activation of pathways favoring folliculo-luteal transition

BMC Genomics ◽

10.1186/s12864-021-07817-6 ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Vengala Rao Yenuganti ◽

Dirk Koczan ◽

Jens Vanselow

Keyword(s):

Oleic Acid ◽

Granulosa Cells ◽

System Development ◽

Circulatory System ◽

Bioinformatic Analysis ◽

Negative Energy ◽

Tissue Remodelling ◽

Gonadotropin Secretion ◽

Genome Wide

Abstract Background Metabolic stress, as negative energy balance on one hand or obesity on the other hand can lead to increased levels of free fatty acids in the plasma and follicular fluid of animals and humans. In an earlier study, we showed that increased oleic acid (OA) concentrations affected the function of cultured bovine granulosa cells (GCs). Here, we focus on genome wide effects of increased OA concentrations. Results Our data showed that 413 genes were affected, of which 197 were down- and 216 up-regulated. Specifically, the expression of FSH-regulated functional key genes, CCND2, LHCGR, INHA and CYP19A1 and 17-β-estradiol (E2) production were reduced by OA treatment, whereas the expression of the fatty acid transporter CD36 was increased and the morphology of the cells was changed due to lipid droplet accumulation. Bioinformatic analysis revealed that associated pathways of the putative upstream regulators “FSH” and “Cg (choriogonadotropin)” were inhibited and activated, respectively. Down-regulated genes are over-represented in GO terms “reproductive structure/system development”, “ovulation cycle process”, and “(positive) regulation of gonadotropin secretion”, whereas up-regulated genes are involved in “circulatory system development”, “vasculature development”, “angiogenesis” or “extracellular matrix/structure organization”. Conclusions From these data we conclude that besides inhibiting GC functionality, increased OA levels seemingly promote angiogenesis and tissue remodelling, thus suggestively initiating a premature fulliculo-luteal transition. In vivo this may lead to impeded folliculogenesis and ovulation, and cause sub-fertility.

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Source of ovarian inhibin secretion during the oestrous cycle of the sheep

Journal of Endocrinology ◽

10.1677/joe.0.1230181 ◽

1989 ◽

Vol 123 (2) ◽

pp. 181-188 ◽

Cited By ~ 19

Author(s):

G. E. Mann ◽

A. S. McNeilly ◽

D. T. Baird

Keyword(s):

Corpus Luteum ◽

Luteal Phase ◽

Venous Blood ◽

Contralateral Side ◽

Follicular Phase ◽

Oestrous Cycle ◽

Secretion Rate ◽

Antral Follicles ◽

Luteal Tissue

ABSTRACT The source of inhibin secretion by the ovary in the sheep at different stages of the oestrous cycle was investigated by in-vivo cannulation of the ovarian veins. Twenty-four Scottish Blackface ewes were allocated to four groups of six ewes, i.e. those operated on during the luteal phase (day 10), and those operated on during the follicular phase 24–30, 36 and 60 h following an injection of 125 μg cloprostenol on day 10 of the luteal phase. Samples of jugular and timed ovarian venous blood were collected under anaesthesia before and after enucleation of the corpus luteum. Ovaries were then removed and follicles dissected out. Following injection of cloprostenol, luteal regression occurred as indicated by a fall in the secretion of progesterone. The concentration of inhibin in jugular venous plasma and its ovarian secretion rate were similar at all stages of the follicular phase and during the luteal phase. In contrast, the secretion rate of oestradiol rose from 2·68 ±0·73 pmol/min during the luteal phase to 8·70± 2·24 pmol/min 24 h after injection of cloprostenol (P<0·05). Following enucleation of the corpus luteum the secretion rate of progesterone fell from 809 ± 270 pmol/min to 86 ± 30 pmol/min (P<0·001). There was also a smaller, artifactual fall in the secretion rate of oestradiol following enucleation of the corpus luteum, which was of similar size to a fall seen in the secretion rate of inhibin. This resulted in a significant (P<0·001) fall in the ratio of progesterone to inhibin, while the oestradiol to inhibin ratio remained unchanged. The secretion rate of inhibin from ovaries containing luteal tissue was similar to that from the contralateral side without luteal tissue (1·41±0·30 compared with 1·32±0·30 ng/min), while ovaries with large antral follicles secreted significantly (P< 0·001) more inhibin than those with no follicles ≥3 mm (2·28 ± 0·36 compared with 0·25 ±0·06 ng/min). From these results we conclude that, in the sheep, large antral follicles are responsible for most, if not all, the secretion of inhibin by the ovary at all stages of the oestrous cycle, and that the corpus luteum secretes little or no immunoactive or bioactive inhibin. Due to the fact that, unlike inhibin, the secretion rate of oestradiol rises during the follicular phase of the cycle, when the concentration of FSH is suppressed, it seems likely that oestradiol rather than inhibin is the major ovarian factor modulating the change in FSH secretion seen at this stage of the oestrous cycle. Journal of Endocrinology (1989) 123, 181–188

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The conflict between hierarchical ovarian follicular development and superovulation treatment

Reproduction ◽

10.1530/rep-10-0165 ◽

2010 ◽

Vol 140 (2) ◽

pp. 287-294 ◽

Cited By ~ 11

Author(s):

Kenneth P McNatty ◽

Derek A Heath ◽

Norma L Hudson ◽

Karen L Reader ◽

Laurel Quirke ◽

...

Keyword(s):

Granulosa Cell ◽

Granulosa Cells ◽

Follicular Development ◽

Follicular Phase ◽

Ovulation Rate ◽

Cell Populations ◽

Antral Follicles ◽

Functional States ◽

Ovarian Follicular Development

In mammals with a low ovulation rate phenotype, ovarian follicular development is thought to be hierarchical with few, if any, antral follicles at similar stages of development. The hypothesis being tested herein was that if most follicles are in a functionally different state, then the application of exogenous hormones to increase ovulation rate will not overcome the hierarchical nature of follicular development. Using sheep as the experimental model, the functional states of all non-atretic antral follicles ≥2 mm diameter were assessed in individual ewes (N=10/group) during anoestrus with or without pregnant mare's serum gonadotrophin (PMSG) treatment, or after a standard superovulation regimen, or during the follicular phase of the oestrous cycle. The functional states of these follicles were assessed by measuring the FSH- or human chorionic gonadotrophin (hCG)-induced cAMP responses of granulosa cellsin vitro. There were significant overall effects across the treatment groups on the responses of granulosa cells to either FSH or LH (bothP<0.001). It was concluded that for anoestrous ewes with or without PMSG treatment, and ewes during the follicular phase, granulosa cell populations of many follicles (≥2 mm diameter) did not share a similar cAMP response to FSH (∼50% of follicles) or hCG (>90% of follicles) either on a per cell or total cell basis. After superovulation, ≤30 and 10% respectively of the granulosa cell populations shared similar responses to FSH and LH with regard to follicular diameter and cAMP output. Thus, exogenous hormone treatments used routinely for increasing oocyte yield do not effectively override the hierarchical pattern of ovarian follicular development during the follicular phase.

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11β-Hydroxysteroid dehydrogenase expression and activities in bovine granulosa cells and corpora lutea implicate corticosteroids in bovine ovarian physiology

Journal of Endocrinology ◽

10.1677/joe.1.07025 ◽

2007 ◽

Vol 193 (2) ◽

pp. 299-310 ◽

Cited By ~ 15

Author(s):

L M Thurston ◽

D R E Abayasekara ◽

A E Michael

Keyword(s):

Molecular Mass ◽

Granulosa Cells ◽

Luteal Phase ◽

Hydroxysteroid Dehydrogenase ◽

Follicular Phase ◽

Corpora Lutea ◽

Luteal Cells ◽

Antral Follicles ◽

Follicle Diameter ◽

Dependent Type

Cortisol–cortisone metabolism is catalysed by the bi-directional NADP(H)-dependent type 1 11β-hydroxysteroid dehydrogenase (11βHSD1) enzyme and the oxidative NAD+-dependent type 2 11βHSD (11βHSD2). This study related the expression of 11βHSD1 and 11βHSD2 enzymes (mRNA and protein) to net 11-ketosteroid reductase and 11β-dehydrogenase (11β-DH) activities in bovine follicular granulosa and luteal cells. Granulosa cells were isolated from follicles of < 4, 4–8, > 8 and > 12 mm in diameter in either the follicular or luteal phase of the ovarian cycle. Luteal cells were obtained from corpora lutea (CL) in the early non-pregnant luteal phase. Enzyme expression was assessed by reverse transcription-PCR and western blotting, while enzyme activities were measured over 1 h in cell homogenates using radiometric conversion assays with 100 nM [3H]cortisone or [3H]cortisol and pyridine dinucleotide cofactors. Irrespective of follicle diameter, the expression of 11βHSD2 and NAD+-dependent oxidation of cortisol predominated in granulosa cells harvested in the follicular phase. In contrast, in granulosa cells obtained from luteal phase follicles and in bovine luteal cells, expression of 11βHSD1 exceeded that of 11βHSD2 and the major enzyme activity was NADP+-dependent cortisol oxidation. Increasing follicular diameter was associated with progressive increases in expression and activities of 11βHSD2 and 11βHSD1 in follicular and luteal phase granulosa cells respectively. In follicular phase granulosa cells from antral follicles < 12 mm, 11βHSD1 migrated with a molecular mass of 34 kDa, whereas in the dominant follicle, CL and all luteal phase granulosa cells, a second protein band of 68 kDa was consistently detected. In all samples, 11βHSD2 had a molecular mass of 48 kDa, but in large antral follicles (> 8 mm), there was an additional immunoreactive band at 50 kDa. We conclude that 11βHSD2 is the predominant functional 11βHSD enzyme expressed in follicular phase granulosa cells from growing bovine antral follicles. In contrast, in bovine granulosa cells from dominant or luteal phase follicles, and in bovine luteal cells from early non-pregnant CL, 11βHSD1 is the major glucocorticoid-metabolising enzyme. The increasing levels of cortisol inactivation by the combined NADP+- and NAD+-dependent 11β-DH activities suggest a need to restrict cortisol access to corticosteroid receptors in the final stages of follicle development.

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XIAP: a potential determinant of ovarian follicular fate

Reproduction ◽

10.1530/rep-12-0142 ◽

2012 ◽

Vol 144 (2) ◽

pp. 165-176 ◽

Cited By ~ 12

Author(s):

Hollian R Phillipps ◽

Peter R Hurst

Keyword(s):

Granulosa Cells ◽

Current Knowledge ◽

Inhibitor Of Apoptosis ◽

Caspase Inhibitor ◽

Follicular Atresia ◽

Inhibitor Of Apoptosis Protein ◽

Apoptosis Protein ◽

Potential Determinant

X-linked inhibitor of apoptosis protein (XIAP), a member of the inhibitor of apoptosis protein family, is involved in regulating a number of functions including receptor-mediated intracellular signalling and early development. Its role as an endogenous caspase inhibitor, however, is the most highly characterised. Consequently, this protein has been implicated as an anti-apoptotic factor in the ovary.In vitroandin vivostudies have begun dissecting the stimuli and signalling networks that lead to XIAP upregulation in granulosa cells. The objective of this review is to briefly summarise the current knowledge concerning XIAP and its interactions with different caspases. Furthermore, XIAP's emerging role in the mammalian ovary will be explored and comparison is made with its functions in the mammary gland. Finally, the idea that XIAP may act as a molecular signalling switch in granulosa cells following detachment from underlying layers to promote follicular atresia will be introduced.

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206.Cell death of the theca interna during bovine ovarian follicular atresia

Reproduction Fertility and Development ◽

10.1071/srb04abs206 ◽

2004 ◽

Vol 16 (9) ◽

pp. 206

Author(s):

L. J. Clark ◽

H. F. Irving-Rodgers ◽

A. M. Dharmarajan ◽

R. J. Rodgers

Keyword(s):

Endothelial Cells ◽

Cell Death ◽

Side Chain ◽

Numerical Density ◽

Follicular Atresia ◽

Antral Follicles ◽

Chain Cleavage ◽

Significant Difference ◽

Steroidogenic Cells ◽

Theca Interna

It is generally accepted that death of cells within the theca interna occurs late during ovarian follicular atresia. Histological classifications of atresia are usually based solely upon the morphology of the membrana granulosa. Atresia of bovine antral follicles less than 5 mm in diameter has been redefined as either antral or basal atresia depending on where in the membrana granulosa cell death is initiated. The aim of present study was to investigate changes within the theca interna during both antral and basal atresia. Bovine ovaries were collected and processed for light microscopy and immunohistochemistry. Each follicle less then 5 mm was classified as either healthy, antral atretic or basal atretic, with antral atresia being further classified either early-mid or late stage. Sections were labelled by TUNEL to identify dead cells combined with lectin from Bandeiraea simplificifolia to identify endothelial cells or with an antibody to cytochrome P450 cholesterol side-chain cleavage to identify steroidogenic cells. The numerical density of steroidogenic cells within the theca interna was significantly reduced (P < 0.001) in basal atretic follicles compared to healthy and antral atretic follicles. In both antral and basal atresia there was death of endothelial cells and steroidogenic cells. However cell death was greater in endothelial cells (P < 0.05) and steroidogenic cells (P < 0.001) of the theca interna of basal atretic follicles. There was no significant difference in the amount of cell death in the membrana granulosa between early-mid antral atresia and basal atresia while death of the membrana granulosa was significantly increased in late antral atresia compared to basal atresia (P < 0.01). Therefore we conclude that basal atresia is not a progression of antral atresia and that the theca interna can be susceptible to cell death early in atresia in basal atretic follicles.

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