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Stem cells, progenitor cells, and lineage decisions in the ovary.

Hummitzsch K, Anderson RA, Wilhelm D, Wu J, Telfer EE, Russell DL, Robertson SA, Rodgers RJ - Endocr. Rev. (2014)

Bottom Line: Similarly, claims of very small embryonic-like cells are also preliminary.Surface epithelial cells originating from gonadal ridge epithelial-like cells and from the mesonephric epithelium at the hilum of the ovary have also been proposed.This review draws together the current evidence and perspectives on this topic.

View Article: PubMed Central - PubMed

Affiliation: Discipline of Obstetrics and Gynaecology (K.H., D.L.R., S.A.R., R.J.R.), School of Paediatrics and Reproductive Health, Robinson Research Institute, University of Adelaide, Adelaide, South Australia, Australia 5005; Medical Research Council Centre for Reproductive Health (R.A.A.), The University of Edinburgh, The Queens Medical Research Institute, Edinburgh EH16 4TJ, United Kingdom; Department of Anatomy and Developmental Biology (D.W.), Monash University, Clayton, Victoria, Australia 3800; Bio-X Institutes (J.W.), Shanghai Jiao Tong University, Shanghai 200240, China; and Institute of Cell Biology and Centre for Integrative Physiology (E.E.T), The University of Edinburgh, Edinburgh EH8 9XE, United Kingdom.

ABSTRACT
Exploring stem cells in the mammalian ovary has unleashed a Pandora's box of new insights and questions. Recent evidence supports the existence of stem cells of a number of the different cell types within the ovary. The evidence for a stem cell model producing mural granulosa cells and cumulus cells is strong, despite a limited number of reports. The recent identification of a precursor granulosa cell, the gonadal ridge epithelial-like cell, is exciting and novel. The identification of female germline (oogonial) stem cells is still very new and is currently limited to just a few species. Their origins and physiological roles, if any, are unknown, and their potential to produce oocytes and contribute to follicle formation in vivo lacks robust evidence. The precursor of thecal cells remains elusive, and more compelling data are needed. Similarly, claims of very small embryonic-like cells are also preliminary. Surface epithelial cells originating from gonadal ridge epithelial-like cells and from the mesonephric epithelium at the hilum of the ovary have also been proposed. Another important issue is the role of the stroma in guiding the formation of the ovary, ovigerous cords, follicles, and surface epithelium. Immune cells may also play key roles in developmental patterning, given their critical roles in corpora lutea formation and regression. Thus, while the cellular biology of the ovary is extremely important for its major endocrine and fertility roles, there is much still to be discovered. This review draws together the current evidence and perspectives on this topic.

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Morphological changes of the granulosa cells and the granulosa layer during follicle development. [Adapted from data derived from P. Da Silva-Buttkus et al: Effect of cell shape and packing density on granulosa cell proliferation and formation of multiple layers during early follicle development in the ovary. J Cell Sci. 2008;121:3890–3900 (271) and from R. J. Rodgers and H. F. Irving-Rodgers: Morphological classification of bovine ovarian follicles. Reproduction. 2010;139:309–318 (272).]
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Figure 6: Morphological changes of the granulosa cells and the granulosa layer during follicle development. [Adapted from data derived from P. Da Silva-Buttkus et al: Effect of cell shape and packing density on granulosa cell proliferation and formation of multiple layers during early follicle development in the ovary. J Cell Sci. 2008;121:3890–3900 (271) and from R. J. Rodgers and H. F. Irving-Rodgers: Morphological classification of bovine ovarian follicles. Reproduction. 2010;139:309–318 (272).]

Mentions: When first formed, the follicle contains oocytes and GREL/pregranulosa cells. It is not known whether there is a distinction between GREL and pregranulosa cells and, if so, at what stage the transition occurs or what initiates it. However, after growth of the primordial follicle is initiated, proliferation commences in the previously quiescent GREL/pregranulosa cells (Figure 6), and they differentiate into granulosa cells whose function in immature follicles is to support the growth of the oocyte. During growth of the bovine follicles, granulosa cells double in number 21 times from the primordial to antral follicle stage (151). The first evidence that some granulosa cells had properties of stem cells came in 1994 (152) when it was proposed that the membrana granulosa, like other epithelia, is derived from stem cells. It was shown that a proportion of granulosa cells isolated directly from antral follicles has a number of stem cell properties, including the ability to divide under anchorage-independent conditions and form colonies (146, 152–155), divide without contact inhibition (151), and express telomerase (156), with the highest activity in the smaller follicles also supporting a stem cell model as proposed (151). The colonies of granulosa cells produced a basal lamina, and the granulosa cells in colonies could be induced to differentiate into luteal cells with dibutyryl cAMP treatment (152), eliminating the possibility that the colonies might have been derived from contaminating blood cells.


Stem cells, progenitor cells, and lineage decisions in the ovary.

Hummitzsch K, Anderson RA, Wilhelm D, Wu J, Telfer EE, Russell DL, Robertson SA, Rodgers RJ - Endocr. Rev. (2014)

Morphological changes of the granulosa cells and the granulosa layer during follicle development. [Adapted from data derived from P. Da Silva-Buttkus et al: Effect of cell shape and packing density on granulosa cell proliferation and formation of multiple layers during early follicle development in the ovary. J Cell Sci. 2008;121:3890–3900 (271) and from R. J. Rodgers and H. F. Irving-Rodgers: Morphological classification of bovine ovarian follicles. Reproduction. 2010;139:309–318 (272).]
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4496428&req=5

Figure 6: Morphological changes of the granulosa cells and the granulosa layer during follicle development. [Adapted from data derived from P. Da Silva-Buttkus et al: Effect of cell shape and packing density on granulosa cell proliferation and formation of multiple layers during early follicle development in the ovary. J Cell Sci. 2008;121:3890–3900 (271) and from R. J. Rodgers and H. F. Irving-Rodgers: Morphological classification of bovine ovarian follicles. Reproduction. 2010;139:309–318 (272).]
Mentions: When first formed, the follicle contains oocytes and GREL/pregranulosa cells. It is not known whether there is a distinction between GREL and pregranulosa cells and, if so, at what stage the transition occurs or what initiates it. However, after growth of the primordial follicle is initiated, proliferation commences in the previously quiescent GREL/pregranulosa cells (Figure 6), and they differentiate into granulosa cells whose function in immature follicles is to support the growth of the oocyte. During growth of the bovine follicles, granulosa cells double in number 21 times from the primordial to antral follicle stage (151). The first evidence that some granulosa cells had properties of stem cells came in 1994 (152) when it was proposed that the membrana granulosa, like other epithelia, is derived from stem cells. It was shown that a proportion of granulosa cells isolated directly from antral follicles has a number of stem cell properties, including the ability to divide under anchorage-independent conditions and form colonies (146, 152–155), divide without contact inhibition (151), and express telomerase (156), with the highest activity in the smaller follicles also supporting a stem cell model as proposed (151). The colonies of granulosa cells produced a basal lamina, and the granulosa cells in colonies could be induced to differentiate into luteal cells with dibutyryl cAMP treatment (152), eliminating the possibility that the colonies might have been derived from contaminating blood cells.

Bottom Line: Similarly, claims of very small embryonic-like cells are also preliminary.Surface epithelial cells originating from gonadal ridge epithelial-like cells and from the mesonephric epithelium at the hilum of the ovary have also been proposed.This review draws together the current evidence and perspectives on this topic.

View Article: PubMed Central - PubMed

Affiliation: Discipline of Obstetrics and Gynaecology (K.H., D.L.R., S.A.R., R.J.R.), School of Paediatrics and Reproductive Health, Robinson Research Institute, University of Adelaide, Adelaide, South Australia, Australia 5005; Medical Research Council Centre for Reproductive Health (R.A.A.), The University of Edinburgh, The Queens Medical Research Institute, Edinburgh EH16 4TJ, United Kingdom; Department of Anatomy and Developmental Biology (D.W.), Monash University, Clayton, Victoria, Australia 3800; Bio-X Institutes (J.W.), Shanghai Jiao Tong University, Shanghai 200240, China; and Institute of Cell Biology and Centre for Integrative Physiology (E.E.T), The University of Edinburgh, Edinburgh EH8 9XE, United Kingdom.

ABSTRACT
Exploring stem cells in the mammalian ovary has unleashed a Pandora's box of new insights and questions. Recent evidence supports the existence of stem cells of a number of the different cell types within the ovary. The evidence for a stem cell model producing mural granulosa cells and cumulus cells is strong, despite a limited number of reports. The recent identification of a precursor granulosa cell, the gonadal ridge epithelial-like cell, is exciting and novel. The identification of female germline (oogonial) stem cells is still very new and is currently limited to just a few species. Their origins and physiological roles, if any, are unknown, and their potential to produce oocytes and contribute to follicle formation in vivo lacks robust evidence. The precursor of thecal cells remains elusive, and more compelling data are needed. Similarly, claims of very small embryonic-like cells are also preliminary. Surface epithelial cells originating from gonadal ridge epithelial-like cells and from the mesonephric epithelium at the hilum of the ovary have also been proposed. Another important issue is the role of the stroma in guiding the formation of the ovary, ovigerous cords, follicles, and surface epithelium. Immune cells may also play key roles in developmental patterning, given their critical roles in corpora lutea formation and regression. Thus, while the cellular biology of the ovary is extremely important for its major endocrine and fertility roles, there is much still to be discovered. This review draws together the current evidence and perspectives on this topic.

Show MeSH
Related in: MedlinePlus