Evidence That the Mechanism of Prenatal Germ Cell Death in the Mouse Is Apoptosis

Coucouvanis, Electra; Sherwood, Sylvia; Carswell-Crumpton, Catherine; Spack, Edward G.; Jones, Patricia P.

doi:10.1006/excr.1993.1307

Cited by 188 publications

(132 citation statements)

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“…Because such cells show defective cytoskeletal organization and cell adhesion, it is possible that similar changes account for the selective release of oocytes from the OSE. In all the mammalian species studied, there is an oversupply of germ cells within the late fetal ovary (Coucouvanis et al 1993, Vaskivuo et al 2001, Vaskivuo & Tapanainen 2002. Depending on the species, many oocytes are eliminated by apoptosis prior to and at the time of birth (Ratts et al 1995, Reynaud & Driancourt 2000, Shirota et al 2003, De Felici 2004, and those that remain in the neonatal mouse ovary acquire and are surrounded by granulosa cells, establishing a pool of diplotene-arrested oocytes identified as primordial follicles (Pedersen 1969, Peters 1969.…”

Section: Discussionmentioning

confidence: 99%

Quantification of healthy follicles in the neonatal and adult mouse ovary: evidence for maintenance of primordial follicle supply

Kerr¹,

Duckett²,

Myers³

et al. 2006

Reproduction

193

180

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Proliferation and partial meiotic maturation of germ cells in fetal ovaries is believed to establish a finite, non-renewable pool of primordial follicles at birth. The supply of primordial follicles in postnatal life should be depleted during folliculogenesis, either undergoing atresia or surviving to ovulation. Recent studies of mouse ovaries propose that intra-and extraovarian germline stem cells replenish oocytes and form new primordial follicles. We quantified all healthy follicles in C57BL/6 mouse ovaries from day 1 to 200 using unbiased stereological methods, immunolabelling of oocyte meiosis (germ cell nuclear antigen (GCNA)) and ovarian cell proliferation (proliferating cell nuclear antigen (PCNA)) and electronmicroscopy. Day 1 ovaries contained 7924G1564 (S.E.M.) oocytes or primordial follicles, declining on day 7 to 1987G203, with 200-800 oocytes ejected from individual ovaries on that day and day 12. Discarded oocytes and those subjacent to the surface epithelium were GCNA-positive indicating their incomplete meiotic maturation. From day 7 to 100 mean numbers of primordial follicles per ovary were not significantly depleted but declined at 200 days to 254G71. Mean numbers of all healthy follicles per ovary were not significantly different from day 7 to 100 (range 2332G349-3007G322). Primordial follicle oocytes were PCNA-negative. Occasional unidentified cells were PCNA-positive with mitotic figures observed in the cortex of day 1 and 12 ovaries. Although we found no evidence for ovarian germline stem cells, our data support the hypothesis of postnatal follicle renewal in postnatal and adult ovaries of C57BL/6 mice. Reproduction (2006) 132 95-109

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Section: Discussionmentioning

confidence: 99%

Quantification of healthy follicles in the neonatal and adult mouse ovary: evidence for maintenance of primordial follicle supply

Kerr¹,

Duckett²,

Myers³

et al. 2006

Reproduction

193

180

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“…Recent flow cytometric analysis of germ cells isolated from fetal mouse gonads has demonstrated that apoptosis is at least one mechanism underlying prenatal oogonium and oocyte loss (Coucouvanis et al, 1993). These in vivo investigations have been supported by several in vitro studies documenting the occurrence of apoptosis by many criteria in primordial germ cells (Pesce et al, 1993;Pesce and De Felici, 1994) and oogonia/oocytes (Martimbeau et al, 1996) following deprivation of serum or cytokines needed for survival in culture.…”

Section: Apoptosis In the Ovary: A Brief Historical Accountmentioning

confidence: 96%

The genes of cell death and cellular susceptibility to apoptosis in the ovary: a hypothesis

Tilly

Perez

1997

Cell Death Differ

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Recent advances in the field of cell death, primarily derived from gene-transfer experiments and manipulation of tumor cell lines in vitro, have identified key genes responsible for determining whether or not a given cell will initiate apoptosis. However, comparatively less is known of the role that the products of these genes play in physiological settings of cell death. In the ovary, a tremendous level of normal cell death takes place in the germline throughout the later stages of fetal development. This process is responsible for setting the absolute number of oocytes (`eggs') available for subsequent development and ovulation during adult life. Interestingly, death remains the fate of the vast majority of oocytes that survive the waves of attrition during fetal life and are endowed in the post-natal ovary as primordial follicles. This pool of oocytes is lost indirectly as a consequence of the death of the somatic (granulosa) cells that, in the case of a small percentage of the total follicles, support and nourish the oocyte until its release at ovulation. Due to the magnitude of cell death that occurs normally within the female gonad during both fetal development and post-natal life, the ovary has proven to be an excellent model to study the role of cell death genes in a physiological setting of endocrine-regulated apoptosis.It is now known that a diverse spectrum of pro-and antiapoptosis susceptibility genes, including members of the bcl-2 and CASP (ced-3/Ice) gene families, are expressed in germ cells and/or somatic cells of the ovary. Many, but not all, of these genes are regulated by specific survival factors, such as gonadotropins and growth factors, and changes in the temporal patterns of cell death gene expression suggest an intimate association exists between the products of these genes and activation of cellular suicide. Moreover, pathological oocyte destruction, such as that triggered by exposure of female germ cells to chemotherapeutic compounds or environmental toxicants, may also be dependent upon genedriven apoptosis. As such, this review will discuss data supporting the hypothesis that the susceptibility of ovarian cells to death induction is dependent upon the pattern of cell death gene expression occurring within those cells prior to and/or concomitant with receipt of the stimulus for apoptosis. Elucidation of the relationship between germ cell loss and cell death genes may allow future intervention into the process of oocyte depletion associated with normal and pathophysiological reproductive senescence.

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“…Death occurs at all stages of oogenesis, but a wave of attrition involving a large proportion of the germ cells present has been documented in the mouse at E13.5-E15.5, when oogonia cease mitosis and enter into meiosis. A second wave of loss occurs during the breakdown of oogonial nests between E17.5 and PN1 in mice, which is coincident with the assembly of oocytes into primordial follicles (Coucouvanis et al 1993, Ratts et al 1995. The strains of mice used by these authors (C57BL and ICR wild-type (WT) female mice respectively) may be significant since variation in oogonial loss is thought to be heavily dependent on genotype.…”

Section: Establishment Of the Ovarian Pool Of Primordial Folliclesmentioning

confidence: 99%

“…The strains of mice used by these authors (C57BL and ICR wild-type (WT) female mice respectively) may be significant since variation in oogonial loss is thought to be heavily dependent on genotype. The germ cells lost during these waves before the formation of oocytes in primordial follicles exhibit nuclear condensation, cell shrinkage and fragmentation, and DNA laddering with positive TUNEL staining, and PARP1 immunoreactivity, all of which are characteristics typically associated with apoptosis (Coucouvanis et al 1993, Pesce & De Felici 1994, Pepling & Spradling 2001, Ghafari et al 2007, Lobascio et al 2007a, 2007b.…”

Section: Establishment Of the Ovarian Pool Of Primordial Folliclesmentioning

confidence: 99%

Apoptosis in the germ line

Aitken¹,

Findlay²,

Hutt³

et al. 2011

Reproduction

159

102

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Apoptosis is a critical process for regulating both the size and the quality of the male and female germ lines. In this review, we examine the importance of this process during embryonic development in establishing the pool of spermatogonial stem cells and primordial follicles that will ultimately define male and female fertility. We also consider the importance of apoptosis in controlling the number and quality of germ cells that eventually determine reproductive success. The biochemical details of the apoptotic process as it affects germ cells in the mature gonad still await resolution, as do the stimuli that persuade these cells to commit to a pathway that leads to cell death. Our ability to understand and ultimately control the reproductive potential of male and female mammals depends upon a deeper understanding of these fundamental processes.

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Evidence That the Mechanism of Prenatal Germ Cell Death in the Mouse Is Apoptosis

Cited by 188 publications

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Quantification of healthy follicles in the neonatal and adult mouse ovary: evidence for maintenance of primordial follicle supply

Quantification of healthy follicles in the neonatal and adult mouse ovary: evidence for maintenance of primordial follicle supply

The genes of cell death and cellular susceptibility to apoptosis in the ovary: a hypothesis

Apoptosis in the germ line

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