Low oocyte mitochondrial DNA content in ovarian insufficiency

May‐Panloup, Pascale; Chrétien, Marie-Françoise; Jacques, Caroline; Vasseur, Claudine; Malthièry, Yves; Reynier, Pascal

doi:10.1093/humrep/deh667

Cited by 267 publications

(220 citation statements)

References 31 publications

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“…Recently, it was reported that there is a very short period of mtDNA synthesis from the 1-cell to 2-cell stage, which can be affected by environmental stress in mice (McConnell & Petrie 2004). Further, May-Panloup et al (2005a, 2005b) observed a decrease of mtDNA copy number during 2-cell to morula stage and the following increase at blastocyst stage in in vitro produced bovine embryo. Overall, mtDNA copy number is expressed as a result of balance between the synthesis and the degradation of mtDNA and in vitro production procedure including IVC could impair the balance.…”

Section: Discussionmentioning

confidence: 96%

“…The mitochondrial copy number has been reported in oocytes from mice (Piko & Taylor 1987, bovines , pigs (El Shourbagy et al 2006) and humans (Steuerwald et al 2000, Reynier et al 2001, May-Panloup et al 2005a) but, to date, there is no report of the mDNA copy number in rat oocytes. Pioneering studies by Piko & Taylor (1987) showed that the quantity of mtDNA remains stable throughout early development in mice, suggesting an absence of mtDNA replication during preimplantation; however, it has been suggested that there is a very short period of mtDNA synthesis immediately after fertilization in mice, which can be affected by environmental stress (McConnell & Petrie 2004).…”

Section: Introductionmentioning

confidence: 99%

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Characterization of mitochondrial replication and transcription control during rat early development in vivo and in vitro

Kameyama

Yoo²,

Smith

2007

Reproduction

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In vitro culture (IVC), used in assisted reproductive technologies, is a major environmental stress on the embryo. To evaluate the effect of IVC on mitochondrial transcription and the control of mtDNA replication, we measured the mtDNA copy number and relative amount of mRNA for mitochondrial-related genes in individual rat oocytes, zygotes and embryos using real-time PCR. The average mtDNA copy number was 147 600 (G3000) in metaphase II oocytes. The mtDNA copy number was stable throughout in vivo early development and IVC induced an increase in mtDNA copy number from the 8-cell stage onwards. Gapd mRNA levels vary during early development and IVC did not change the patterns of these housekeeping gene transcripts. Polrmt mRNA levels did not vary during early development up to the morula stage but increased at the blastocyst stage. IVC induced the up-regulation of Polrmt mRNA, one of the key genes regulating mtDNA transcription and replication, at the blastocyst stage. An increase in mt-Nd4 mRNA preceded the blastocyst-related event observed in nuclear-encoded Gapd and Polrmt, suggesting that the expression of mitochondrial encoded genes is controlled differently from nuclear encoded genes. We conclude that the IVC system can perturb mitochondrial transcription and the control of mtDNA replication in rat embryos. This perturbation of mtDNA regulation may be responsible for the abnormal physiology, metabolism and viability of in vitro-derived embryos.

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Section: Discussionmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

Characterization of mitochondrial replication and transcription control during rat early development in vivo and in vitro

Kameyama

Yoo²,

Smith

2007

Reproduction

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“…Equally impressive, however, is the substantial accumulation of mitochondrial (mt) DNA (Dumollard et al 2007, St John et al 2010, Van Blerkom 2010. Although there is some variability among reports, particularly in humans, current data indicate that a mature fertilizable mammalian oocyte harbors 150 000-250 000 copies of mtDNA depending on the species (mouse (Piko & Taylor 1987, Cao et al 2007, human (Steuerwald et al 2000, Reynier et al 2001, Barritt et al 2002, May-Panloup et al 2005, Santos et al 2006, Zeng et al 2007, cow (May-Panloup et al 2007), pig , and rat (Kameyama et al 2007)). As, at least in the mouse, primordial germ cells in the gonad contain about 2000 copies (Cao et al 2007, Wai et al 2008, it may be estimated that during mammalian oogenesis mtDNA content increases about 100-fold.…”

Section: Introductionmentioning

confidence: 99%

Regulation of mitochondrial DNA accumulation during oocyte growth and meiotic maturation in the mouse

Mahrous¹,

Yang²,

Clarke³

2012

Reproduction

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Oocytes accumulate an enormous quantity of mitochondrial (mt) DNA, and an insufficient amount of mtDNA may underlie some cases of poor oocyte quality leading to infertility. Little is known, however, about the mechanisms that govern the timing and regulation of mtDNA accumulation during oogenesis. We report, through analysis of the mtDNA content of individual oocytes of the mouse, that mtDNA accumulates steadily during oocyte growth to reach a value of w175 000 copies per cell. MtDNA content ceases to increase once oocytes reach full size and remains unchanged during meiotic maturation. To test whether mtDNA accumulation depends on oocyte growth, we inhibited growth in vitro in two ways -by exposing complexes comprising partially grown oocytes enclosed by granulosa cells to a chemical inhibitor of the phosphatidylinositol-3-kinase signaling pathway and by removing the surrounding granulosa cells from partially grown oocytes. Under both conditions, the oocytes fail to grow, but mtDNA accumulation is unaffected, indicating that the two processes can be mechanistically uncoupled. Quantitative analysis of the mRNAs encoding proteins required for mtDNA replication revealed that Polg (Polga) (polymerase-g, a-subunit), Polg2 (Polgb), and Tfam (transcription factor A, mitochondrial) increase during oocyte growth but then decrease after fully grown oocytes become transcriptionally silent as indicated by the non-surrounded nucleolusto-surrounded nucleolus transition. Thus, there is a correlation between the decline in the quantity of mRNAs encoding mtDNA replication factors in fully grown oocytes and the arrest of mtDNA accumulation in these cells, suggesting that the two events may be causally linked.

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“…Gametes of mice were estimated to contain 10-75 and 1.6 Â 10 5 mtDNA molecules per single sperm and oocyte, respectively (Hecht et al, 1984;Shitara et al, 2000;Steuerwald et al, 2000). Human sperm were estimated to contain 1.4-6.8 molecules (MayPanloup et al, 2003;Amaral et al, 2007) and oocytes 1.93-7.95 Â 10 5 mtDNAs (Steuerwald et al, 2000;Reynier et al, 2001;Barritt et al, 2002;Chan et al, 2005;May-Panloup et al, 2005a;Santos et al, 2006). These estimates lead to ratios of 1:5.7 Â 10 5 -1:2.8 Â 10 4 of paternal-to-maternal mtDNA in human and 1:1.6 Â 10 4 -1:2.1 Â 10 3 in mouse zygotes if paternal mtDNA enters the egg upon fertilization.…”

Section: Introductionmentioning

confidence: 99%

Lost in the zygote: the dilution of paternal mtDNA upon fertilization

Wolff¹,

Gemmell²

2008

Heredity

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The mechanisms by which paternal inheritance of mitochondrial DNA (mtDNA) (paternal leakage) and, subsequently, recombination of mtDNA are prevented vary in a speciesspecific manner with one mechanism in common: paternally derived mtDNA is assumed to be vastly outnumbered by maternal mtDNA in the zygote. To date, this dilution effect has only been described for two mammalian species, human and mouse. Here, we estimate the mtDNA content of chinook salmon oocytes to evaluate the dilution effect operating in another vertebrate; the first such study outside a mammalian system. Employing real-time PCR, we determined the mtDNA content of chinook salmon oocytes to be 3.2 Â 10 9 ± 1.0 Â 10 9 , and recently, we determined the mtDNA content of chinook salmon sperm to be 5.73 ± 2.28 per gamete. Accordingly, the ratio of paternal-to-maternal mtDNA if paternal leakage occurs is estimated to be 1:5.5 Â 10 8 . This contribution of paternal mtDNA to the overall mtDNA pool in salmon zygotes is three to five orders of magnitude smaller than those revealed for the mammalian system, strongly suggesting that paternal inheritance of mtDNA per offspring will be much less likely in this system than in mammals.

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Low oocyte mitochondrial DNA content in ovarian insufficiency

Abstract: Our results suggest that low mtDNA content is associated with the impaired oocyte quality observed in ovarian insufficiency.

Cited by 267 publications

References 31 publications

Characterization of mitochondrial replication and transcription control during rat early development in vivo and in vitro

Characterization of mitochondrial replication and transcription control during rat early development in vivo and in vitro

Regulation of mitochondrial DNA accumulation during oocyte growth and meiotic maturation in the mouse

Lost in the zygote: the dilution of paternal mtDNA upon fertilization

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