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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: 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.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.

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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Schematic diagram of ovarian development. [Reproduced from K. Hummitzsch et al: A new model of development of the mammalian ovary and follicles. PloS One. 2013;8:e55578 (31), with permission.]. Abbreviations: CK19, cytokeratin 19; DAPI, 4',6-diamidino-2-phenylindole.
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Figure 4: Schematic diagram of ovarian development. [Reproduced from K. Hummitzsch et al: A new model of development of the mammalian ovary and follicles. PloS One. 2013;8:e55578 (31), with permission.]. Abbreviations: CK19, cytokeratin 19; DAPI, 4',6-diamidino-2-phenylindole.

Mentions: A more recent examination of bovine ovarian development suggests that granulosa cells are not derived from differentiated ovarian surface epithelial cells. Instead, both the apical ovarian surface epithelium and the granulosa cells arise from a precursor population of GREL cells (31) (Figure 4). GREL cells are postulated to be derived from cells of the surface of the mesonephros (31), which replicate to form the genital ridge/ovarian primordium into which the PGCs migrate. Soon afterward, cords of stromal cells referred to as “cell streams” penetrate the primordium from the underlying mesonephros, partitioning the developing ovary into irregularly shaped ovigerous cords composed of GREL cells and PGCs/oogonia. A basal lamina is formed and separates the stromal cells from the ovigerous cords, which at this stage contain GREL cells and oogonial “nests” or small syncytial groups of germ cells that have not completed cytokinesis (31). As development progresses, apoptosis of oogonia occurs, and the oogonial nests are reduced to individual oocytes surrounded by a finite number of GREL cells to form primordial follicles. The basal lamina, which had previously separated the ovigerous cords from the surrounding stroma, now surrounds individual follicles. This interaction with the stroma is a key aspect of follicle formation that has received little attention. There is thus a complex three-way interaction between the oogonia, GREL cells, and the stroma that ultimately determines the number and potentially the quality of follicles with which the ovary is endowed.


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)

Schematic diagram of ovarian development. [Reproduced from K. Hummitzsch et al: A new model of development of the mammalian ovary and follicles. PloS One. 2013;8:e55578 (31), with permission.]. Abbreviations: CK19, cytokeratin 19; DAPI, 4',6-diamidino-2-phenylindole.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Schematic diagram of ovarian development. [Reproduced from K. Hummitzsch et al: A new model of development of the mammalian ovary and follicles. PloS One. 2013;8:e55578 (31), with permission.]. Abbreviations: CK19, cytokeratin 19; DAPI, 4',6-diamidino-2-phenylindole.
Mentions: A more recent examination of bovine ovarian development suggests that granulosa cells are not derived from differentiated ovarian surface epithelial cells. Instead, both the apical ovarian surface epithelium and the granulosa cells arise from a precursor population of GREL cells (31) (Figure 4). GREL cells are postulated to be derived from cells of the surface of the mesonephros (31), which replicate to form the genital ridge/ovarian primordium into which the PGCs migrate. Soon afterward, cords of stromal cells referred to as “cell streams” penetrate the primordium from the underlying mesonephros, partitioning the developing ovary into irregularly shaped ovigerous cords composed of GREL cells and PGCs/oogonia. A basal lamina is formed and separates the stromal cells from the ovigerous cords, which at this stage contain GREL cells and oogonial “nests” or small syncytial groups of germ cells that have not completed cytokinesis (31). As development progresses, apoptosis of oogonia occurs, and the oogonial nests are reduced to individual oocytes surrounded by a finite number of GREL cells to form primordial follicles. The basal lamina, which had previously separated the ovigerous cords from the surrounding stroma, now surrounds individual follicles. This interaction with the stroma is a key aspect of follicle formation that has received little attention. There is thus a complex three-way interaction between the oogonia, GREL cells, and the stroma that ultimately determines the number and potentially the quality of follicles with which the ovary is endowed.

Bottom Line: 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.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.

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