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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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Localization of extracellular matrix components in the stroma of fetal and adult bovine ovaries. A and B, Localization of fibrillin 3 (green) with the stromal cell marker COUP-TFII/NR2F2 (red) in fetal ovaries at gestational days 96 (A) and 182 (B). C, Fibrillin 1 expression (red) and components of laminin 111 (green) in fetal ovary at gestational day 79. D, Fibrillin 1 (green) localization in adult ovary. E, Localization of decorin fibers (green) and components of laminin 111 (red) in fetal ovary at gestational day 79. F, Localization of decorin fibers (green) in adult ovary. Nuclei are counterstained with DAPI (4',6-diamidino-2-phenylindole; blue). Scale bars, A and D, 25 μm; B, C, E, and F, 50 μm. [Panels A and B were 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, and staining in panels C, E, and F was conducted as reported previously in the same article. Panel D was reproduced from M. J. Prodoehl et al: Fibrillins and latent TGFβ binding proteins in bovine ovaries of offspring following high or low protein diets during pregnancy of dams. Mol Cell Endocrinol. 2009;307:133–141 (98), with permission. Elsevier.]
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Figure 2: Localization of extracellular matrix components in the stroma of fetal and adult bovine ovaries. A and B, Localization of fibrillin 3 (green) with the stromal cell marker COUP-TFII/NR2F2 (red) in fetal ovaries at gestational days 96 (A) and 182 (B). C, Fibrillin 1 expression (red) and components of laminin 111 (green) in fetal ovary at gestational day 79. D, Fibrillin 1 (green) localization in adult ovary. E, Localization of decorin fibers (green) and components of laminin 111 (red) in fetal ovary at gestational day 79. F, Localization of decorin fibers (green) in adult ovary. Nuclei are counterstained with DAPI (4',6-diamidino-2-phenylindole; blue). Scale bars, A and D, 25 μm; B, C, E, and F, 50 μm. [Panels A and B were 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, and staining in panels C, E, and F was conducted as reported previously in the same article. Panel D was reproduced from M. J. Prodoehl et al: Fibrillins and latent TGFβ binding proteins in bovine ovaries of offspring following high or low protein diets during pregnancy of dams. Mol Cell Endocrinol. 2009;307:133–141 (98), with permission. Elsevier.]

Mentions: It is becoming apparent that the stroma plays a number of pivotal roles in the ovary. The extent of stroma and its marker (COUP-TFII/NR2F2) and extracellular matrices (fibrillins and decorin) is illustrated in Figure 2. During the formation of the ovary, the stroma penetrates from the mesonephros into the gonadal ridge/ovarian primordium, then composed of gonadal ridge epithelial-like (GREL) cells (58, 81) and PGCs. During penetration, the stroma branches, and this process creates areas of stroma alternating with areas of GREL cells/germ cells and hence produces the ovigerous cords, which are composed of GREL cells and germ cells. These cords are therefore initially “open” to the surface. The penetrating stroma has been observed previously and described as “cell streams” (82). At all times, there is continuous basal lamina between the stroma and the ovigerous cords, between the stroma and follicles, and between the stroma and the surface epithelium. The composition of the basal laminas in these locations is identical. They contain components of laminin 111, collagens type IV and XVIII, perlecan, and nidogens 1 and 2. This supports the notion that cords, follicles, and surface epithelium are formed or compartmentalized by the penetrating stroma, and this highlights an underappreciated role of the stroma in the ovary.


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)

Localization of extracellular matrix components in the stroma of fetal and adult bovine ovaries. A and B, Localization of fibrillin 3 (green) with the stromal cell marker COUP-TFII/NR2F2 (red) in fetal ovaries at gestational days 96 (A) and 182 (B). C, Fibrillin 1 expression (red) and components of laminin 111 (green) in fetal ovary at gestational day 79. D, Fibrillin 1 (green) localization in adult ovary. E, Localization of decorin fibers (green) and components of laminin 111 (red) in fetal ovary at gestational day 79. F, Localization of decorin fibers (green) in adult ovary. Nuclei are counterstained with DAPI (4',6-diamidino-2-phenylindole; blue). Scale bars, A and D, 25 μm; B, C, E, and F, 50 μm. [Panels A and B were 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, and staining in panels C, E, and F was conducted as reported previously in the same article. Panel D was reproduced from M. J. Prodoehl et al: Fibrillins and latent TGFβ binding proteins in bovine ovaries of offspring following high or low protein diets during pregnancy of dams. Mol Cell Endocrinol. 2009;307:133–141 (98), with permission. Elsevier.]
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Localization of extracellular matrix components in the stroma of fetal and adult bovine ovaries. A and B, Localization of fibrillin 3 (green) with the stromal cell marker COUP-TFII/NR2F2 (red) in fetal ovaries at gestational days 96 (A) and 182 (B). C, Fibrillin 1 expression (red) and components of laminin 111 (green) in fetal ovary at gestational day 79. D, Fibrillin 1 (green) localization in adult ovary. E, Localization of decorin fibers (green) and components of laminin 111 (red) in fetal ovary at gestational day 79. F, Localization of decorin fibers (green) in adult ovary. Nuclei are counterstained with DAPI (4',6-diamidino-2-phenylindole; blue). Scale bars, A and D, 25 μm; B, C, E, and F, 50 μm. [Panels A and B were 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, and staining in panels C, E, and F was conducted as reported previously in the same article. Panel D was reproduced from M. J. Prodoehl et al: Fibrillins and latent TGFβ binding proteins in bovine ovaries of offspring following high or low protein diets during pregnancy of dams. Mol Cell Endocrinol. 2009;307:133–141 (98), with permission. Elsevier.]
Mentions: It is becoming apparent that the stroma plays a number of pivotal roles in the ovary. The extent of stroma and its marker (COUP-TFII/NR2F2) and extracellular matrices (fibrillins and decorin) is illustrated in Figure 2. During the formation of the ovary, the stroma penetrates from the mesonephros into the gonadal ridge/ovarian primordium, then composed of gonadal ridge epithelial-like (GREL) cells (58, 81) and PGCs. During penetration, the stroma branches, and this process creates areas of stroma alternating with areas of GREL cells/germ cells and hence produces the ovigerous cords, which are composed of GREL cells and germ cells. These cords are therefore initially “open” to the surface. The penetrating stroma has been observed previously and described as “cell streams” (82). At all times, there is continuous basal lamina between the stroma and the ovigerous cords, between the stroma and follicles, and between the stroma and the surface epithelium. The composition of the basal laminas in these locations is identical. They contain components of laminin 111, collagens type IV and XVIII, perlecan, and nidogens 1 and 2. This supports the notion that cords, follicles, and surface epithelium are formed or compartmentalized by the penetrating stroma, and this highlights an underappreciated role of the stroma in the ovary.

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