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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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Illustration of the conceptual processes needed to derive granulosa cells from the ovarian surface epithelium. There has been no discussion of these processes in the literature or any evidence to identify that they occur. Surface epithelial cells with a basal lamina and stromal interface (A) would first need to undergo an epithelial-mesenchymal transition (B) to break through the surface epithelial basal lamina and to become migratory and migrate to the oogonium (B). They would then need to undergo a mesenchymal-epithelial transition to form epithelial granulosa cells of follicles all enclosed by the follicular basal lamina (C).
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Figure 3: Illustration of the conceptual processes needed to derive granulosa cells from the ovarian surface epithelium. There has been no discussion of these processes in the literature or any evidence to identify that they occur. Surface epithelial cells with a basal lamina and stromal interface (A) would first need to undergo an epithelial-mesenchymal transition (B) to break through the surface epithelial basal lamina and to become migratory and migrate to the oogonium (B). They would then need to undergo a mesenchymal-epithelial transition to form epithelial granulosa cells of follicles all enclosed by the follicular basal lamina (C).

Mentions: The origins of somatic granulosa cells attract considerable conjecture. Granulosa cells were originally considered to be derived from the mesonephric tubules and more recently from the ovarian surface epithelium (reviewed in Refs. 19 and 20). The mesonephros is a complex structure with many different cell types, including stromal cells, endothelial cells, and the different epithelia associated with its nephrons. In mammals, the mesonephros is a transient organ during fetal development, and it develops differently between males and females (101–107) (for reviews see Refs. 108 and 109). In females, it contributes tubules to the hilum and medulla of the ovary, and these persist into adulthood, referred to as the rete ovarii. The evidence that these structures give rise to granulosa cells came from early observations that rete ovarii can have a close association with oocytes (110, 111). This was further strengthened by demonstration that the presence of rete ovarii correlated with the onset of meiosis (112) and follicle formation (113). Subsequently it was suggested that cells derived from the ovarian surface epithelium give rise to the granulosa cells during follicle formation (82, 114). Part of the confusion about the origins of granulosa cells from surface epithelial cells could be clarified by the use of correct terminology. A simple classic epithelium, such as the mature ovarian surface epithelium, consists of a single layer of epithelial cells with an underlying basal lamina at the interface with stroma. If granulosa cells are derived from classic ovarian surface epithelial cells, as opposed to cells located at the surface (no underlying basal lamina and no epithelial-stroma interface), then presumably the surface epithelial cells would need to undergo an epithelial-mesenchymal transition followed by a mesenchymal-epithelial transition, as illustrated in Figure 3—a process for which no evidence exists. With the model of GREL cells as proposed in the bovine (31), the gonadal ridge/ovarian primordium is initially not covered by a classic surface epithelium; instead it is covered by GREL cells that are located at the surface. Thus, we suggest that a way forward is to interpret existing publications to mean that granulosa cells are derived from cells on the surface of the ovary rather than specifically from a classic surface epithelium.


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)

Illustration of the conceptual processes needed to derive granulosa cells from the ovarian surface epithelium. There has been no discussion of these processes in the literature or any evidence to identify that they occur. Surface epithelial cells with a basal lamina and stromal interface (A) would first need to undergo an epithelial-mesenchymal transition (B) to break through the surface epithelial basal lamina and to become migratory and migrate to the oogonium (B). They would then need to undergo a mesenchymal-epithelial transition to form epithelial granulosa cells of follicles all enclosed by the follicular basal lamina (C).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Illustration of the conceptual processes needed to derive granulosa cells from the ovarian surface epithelium. There has been no discussion of these processes in the literature or any evidence to identify that they occur. Surface epithelial cells with a basal lamina and stromal interface (A) would first need to undergo an epithelial-mesenchymal transition (B) to break through the surface epithelial basal lamina and to become migratory and migrate to the oogonium (B). They would then need to undergo a mesenchymal-epithelial transition to form epithelial granulosa cells of follicles all enclosed by the follicular basal lamina (C).
Mentions: The origins of somatic granulosa cells attract considerable conjecture. Granulosa cells were originally considered to be derived from the mesonephric tubules and more recently from the ovarian surface epithelium (reviewed in Refs. 19 and 20). The mesonephros is a complex structure with many different cell types, including stromal cells, endothelial cells, and the different epithelia associated with its nephrons. In mammals, the mesonephros is a transient organ during fetal development, and it develops differently between males and females (101–107) (for reviews see Refs. 108 and 109). In females, it contributes tubules to the hilum and medulla of the ovary, and these persist into adulthood, referred to as the rete ovarii. The evidence that these structures give rise to granulosa cells came from early observations that rete ovarii can have a close association with oocytes (110, 111). This was further strengthened by demonstration that the presence of rete ovarii correlated with the onset of meiosis (112) and follicle formation (113). Subsequently it was suggested that cells derived from the ovarian surface epithelium give rise to the granulosa cells during follicle formation (82, 114). Part of the confusion about the origins of granulosa cells from surface epithelial cells could be clarified by the use of correct terminology. A simple classic epithelium, such as the mature ovarian surface epithelium, consists of a single layer of epithelial cells with an underlying basal lamina at the interface with stroma. If granulosa cells are derived from classic ovarian surface epithelial cells, as opposed to cells located at the surface (no underlying basal lamina and no epithelial-stroma interface), then presumably the surface epithelial cells would need to undergo an epithelial-mesenchymal transition followed by a mesenchymal-epithelial transition, as illustrated in Figure 3—a process for which no evidence exists. With the model of GREL cells as proposed in the bovine (31), the gonadal ridge/ovarian primordium is initially not covered by a classic surface epithelium; instead it is covered by GREL cells that are located at the surface. Thus, we suggest that a way forward is to interpret existing publications to mean that granulosa cells are derived from cells on the surface of the ovary rather than specifically from a classic surface epithelium.

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