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      Phenotypes of the ovarian follicular basal lamina predict developmental competence of oocytes

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          Abstract

          BACKGROUND

          The ovarian follicular basal lamina underlies the epithelial membrana granulosa and maintains the avascular intra-follicular compartment. Additional layers of basal lamina occur in a number of pathologies, including pili annulati and diabetes. We previously found additional layers of follicular basal lamina in a significant percentage of healthy bovine follicles. We wished to determine if this phenomenon existed in humans, and if it was related to oocyte function in the bovine.

          METHODS AND RESULTS

          We examined follicles from human ovaries ( n = 18) by electron microscopy and found that many follicles had additional layers of basal lamina. Oocytes ( n = 222) from bovine follicles with normal or unusual basal laminas were isolated and their ability to undergo in vitro maturation, fertilization and culture to blastocyst was compared. Healthy bovine follicles with a single layer of basal lamina had oocytes with significantly ( P < 0.01) greater developmental competence than healthy follicles with additional layers of follicular basal lamina (65% versus 28%).

          CONCLUSIONS

          These findings provide direct evidence that the phenotype of the follicular basal lamina is related to oocyte competence.

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          Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins.

          Jeremy G B Thompson, Haitham T. Hussein, F Amato … (2005)
          Paracrine factors secreted by the oocyte regulate a broad range of cumulus cell functions. Characteristically, cumulus cells have a low incidence of apoptosis and we proposed that this is due to oocyte-secreted factors acting in an anti-apoptotic manner. Bovine cumulus-oocyte complexes (COC) were aspirated from abattoir-derived ovaries and oocytectomized (OOX) by microsurgical removal of the oocyte. OOX were treated with doses of either denuded oocytes (DO) or various growth factors for 24 hours (+/- rFSH; 0.1 IU/ml). Proportions of apoptotic cumulus cells were assessed using TUNEL and laser confocal scanning microscopy followed by image analysis. Quantification of Bcl-2 and Bax proteins in OOX was undertaken by western analysis. Oocyte removal led to a significant increase in cumulus cell apoptosis compared with COC controls (35% versus 9% TUNEL positive, respectively; P<0.001). Levels of OOX apoptosis were significantly reversed (P<0.001) in a dose-dependent manner when co-cultured with oocytes. Furthermore, the anti-apoptotic effect of oocyte-secreted factors followed a gradient from the site of the oocyte(s). Growth differentiation factor 9 (GDF9) had no significant effect on cumulus cell apoptosis. By contrast, cumulus cell apoptosis was significantly (P<0.001) reduced by bone morphogenetic proteins (BMP) 15, 6 or 7. Accordingly, levels of anti-apoptotic Bcl-2 were high in OOX+DO and OOX+BMP15 and low with OOX+GDF9 or OOX alone, whereas the reverse was observed for pro-apoptotic Bax. DO, BMP15 and BMP6 were also able to protect cumulus cells from undergoing apoptosis induced by staurosporine. FSH partially prevented apoptosis in all treatment groups (P<0.001). Follistatin and a BMP6 neutralizing antibody, which antagonized the anti-apoptotic effects of BMP15 and BMP6, respectively, whether alone or combined, blocked approximately 50% of the anti-apoptotic actions of oocytes. These results are the first to demonstrate that oocyte-secreted factors, and particularly BMP15 and BMP6, maintain the low incidence of cumulus cell apoptosis by establishing a localized gradient of bone morphogenetic proteins.
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            Morphology and morphogenesis of the Stein-Leventhal ovary and of so-called "hyperthecosis".

            P E Hughesdon (1982)
            A study of 34 full-thickness Stein-Leventhal ovarian wedges and 30 age-matched control ovaries allowed comparison of the entire ovarian cross-sections and quantification of their features. As compared with controls, Stein-Leventhal ovaries showed on average (i) double the cross-sectional area, (II) the same number of primordial follicles, (iii) double the number of ripening and subsequent atretic follicles from the earliest stages, (iv) a tunica increased by 50 per cent and more collagenized, (v) cortical stromal thickness increased by a third, (vi) subcortical stroma, whether deep cortical or medullary in site, increased five times, (vii) ovarian hilus cell nests four times as frequently. The increased subcortical stroma was derived partly from the regressive conversion into stroma of the over-numerous older follicles, so augmenting steadily with duration, and partly from a concurrent stromal hyperplasia. Stromal smooth muscle and lutein cell nests were each found in four-fifths of cases. So-called "hyperthecosis," in which such nests are combined with marked stromal increase, is arguably just a late stage of Stein-Leventhal morphology. The whole picture may result directly or indirectly from the raised LH output, although androgens possibly promote early follicle ripening.
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              Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns.

              D Rizos, Kelly M Boland, T Fair … (2003)
              In general, the majority of immature bovine oocytes fail to develop to the blastocyst stage following maturation, fertilization and culture in vitro. The evidence suggests that while culture conditions during in vitro embryo production can impact on the developmental potential of the early embryo, the intrinsic quality of the oocyte is the key factor determining the proportion of oocytes developing to the blastocyst stage. In addition, evidence suggests that the period of post-fertilization embryo culture is the most critical in determining blastocyst quality. This paper reviews the current literature, with emphasis on the bovine model, demonstrating evidence for an effect of oocyte origin and/or in vitro maturation conditions on the developmental capacity and gene expression patterns in the oocyte. Furthermore, the well-documented effects of post-fertilization culture environment on embryo gene expression and quality are highlighted.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Hum Reprod
                Journal ID (publisher-id): humrep
                Journal ID (hwp): humrep
                Title: Human Reproduction (Oxford, England)
                Publisher: Oxford University Press
                ISSN (Print): 0268-1161
                ISSN (Electronic): 1460-2350
                Publication date (Print): April 2009
                Publication date (Electronic): 18 December 2008
                Publication date PMC-release: 18 December 2008
                Volume: 24
                Issue: 4
                Pages: 936-944
                Affiliations
                [1 ]Research Centre for Reproductive Health, School of Paediatrics and Reproductive Health, University of Adelaide , Adelaide, Australia
                [2 ]South Australian Research and Development Institute, Turretfield Research Centre , Rosedale, South Australia 5350, Australia
                [3 ]Gynaecological Oncology, Royal Adelaide Hospital , South Australia, Australia
                [4 ]Basic Medical Sciences and Clinical Developmental Sciences, St. George's, University of London , London SW17 0RE, UK
                [5 ]Present address: Australian Stem Cell Centre, University of Queensland , Brisbane QLD 4072, Australia
                Author notes
                [6 ]Correspondence address. Tel: +61 883033932; Fax: +61 883034099; E-mail: ray.rodgers@ 123456adelaide.edu.au
                Article
                Publisher ID: den447
                DOI: 10.1093/humrep/den447
                PMC ID: 2656928
                PubMed ID: 19095662
                SO-VID: 739ada92-c388-41e1-9bf7-a0488e1ef573
                Copyright © © The Author 2008. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org
                License:

                The online version of this article has been published under an open access model. Users are entitled to use, reproduce, disseminate, or display the open access version of this article for non-commercial purposes provided that: the original authorship is properly and fully attributed: the Journal and Oxford University Press are attributed as the original place of publication with the correct citation details given: if an article is subsequently reproduced or disseminated not in its entirety but only in part or as a derivative word this must be clearly indicated. For commercial re-use, please contact journals.permissions@oxfordjournals.org

                History
                Date received : 22 April 2008
                Date revision received : 11 November 2008
                Date accepted : 15 November 2008
                Categories
                Subject: Original Articles
                Subject: Reproductive Biology

                ScienceOpen disciplines: Human biology
                Keywords: basal lamina,oocyte competence,ovary,in vitro production
                Data availability:
                ScienceOpen disciplines: Human biology
                Keywords: basal lamina, oocyte competence, ovary, in vitro production

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