Increase of mitochondrial DNA content and transcripts in early bovine embryogenesis associated with upregulation of mtTFA and NRF1 transcription factors

May‐Panloup, Pascale; Vignon, Xavier; Chrétien, Marie-Françoise; Heyman, Yvan; Tamassia, M.; Malthièry, Yves; Reynier, Pascal

doi:10.1186/1477-7827-3-65

Cited by 149 publications

(79 citation statements)

References 39 publications

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“…During early development, the mitochondria in a blastomere are distributed sequentially over the newly formed daughter cells, leading to falling numbers of mitochondria per cell until replication is restarted (i.e. at the time of gastrulation in the mouse (Facucho-Oliveira et al 2007) and at blastocyst formation in cattle and pigs (May-Panloup et al 2005b;Spikings et al 2007)). …”

Section: Discussionmentioning

confidence: 99%

“…John et al 2010). Expression of these genes is normally upregulated when mtDNA replication is reactivated (Pikó and Taylor 1987;May-Panloup et al 2005b;Thundathil et al 2005;Spikings et al 2007). Glutathione peroxidase (GPX) and ATP synthase (ATP synthase-coupling factor 6, mitochondrial-like (ATPsynth_F6)) are enzymes involved in balancing the generation and decomposition of ROS (Ufer and Wang 2011) to help prevent ROS levels reaching a point likely to induce oxidative damage.…”

Section: Introductionmentioning

confidence: 99%

“…mouse and rat; Thundathil et al 2005;Kameyama et al 2007;Wai et al 2010) or decreases over time (e.g. cow and pig; May-Panloup et al 2005b;Spikings et al 2007). Mitochondrial replication is not reinitiated until the blastocyst stage in the cow and pig (May-Panloup et al 2005b;Spikings et al 2007) or until gastrulation in the mouse (Facucho-Oliveira et al 2007).…”

Section: Introductionmentioning

confidence: 99%

“…cow and pig; May-Panloup et al 2005b;Spikings et al 2007). Mitochondrial replication is not reinitiated until the blastocyst stage in the cow and pig (May-Panloup et al 2005b;Spikings et al 2007) or until gastrulation in the mouse (Facucho-Oliveira et al 2007). This temporary arrest in mitochondrial replication, despite a near exponential increase in the number of cells, underlines why the number of functional mitochondria present in a mature oocyte is of critical importance for subsequent developmental competence (May-Panloup et al 2007).…”

Section: Introductionmentioning

confidence: 99%

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Maternal age and in vitro culture affect mitochondrial number and function in equine oocytes and embryos

Hendriks¹,

Colleoni²,

Galli³

et al. 2015

Reprod. Fertil. Dev.

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Abstract. Advanced maternal age and in vitro embryo production (IVP) predispose to pregnancy loss in horses. We investigated whether mare age and IVP were associated with alterations in mitochondrial (mt) DNA copy number or function that could compromise oocyte and embryo development. Effects of mare age (,12 vs $12 years) on mtDNA copy number, ATP content and expression of genes involved in mitochondrial replication (mitochondrial transcription factor (TFAM ), mtDNA polymerase g subunit B (mtPOLB) and mitochondrial single-stranded DNA-binding protein (SSB)), energy production (ATP synthase-coupling factor 6, mitochondrial-like (ATP-synth_F6)) and oxygen free radical scavenging (glutathione peroxidase 3 (GPX3)) were investigated in oocytes before and after in vitro maturation (IVM), and in early embryos. Expression of TFAM, mtPOLB and ATP-synth-F6 declined after IVM (P , 0.05). However, maternal age did not affect oocyte ATP content or expression of genes involved in mitochondrial replication or function. Day 7 embryos from mares $12 years had fewer mtDNA copies (P ¼ 0.01) and lower mtDNA : total DNA ratios (P , 0.01) than embryos from younger mares, indicating an effect not simply due to lower cell number. Day 8 IVP embryos had similar mtDNA copy numbers to Day 7 in vivo embryos, but higher mtPOLB (P ¼ 0.013) and a tendency to reduced GPX3 expression (P ¼ 0.09). The lower mtDNA number in embryos from older mares may compromise development, but could be an effect rather than cause of developmental retardation. The general down-regulation of genes involved in mitochondrial replication and function after IVM may compromise resulting embryos.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Maternal age and in vitro culture affect mitochondrial number and function in equine oocytes and embryos

Hendriks¹,

Colleoni²,

Galli³

et al. 2015

Reprod. Fertil. Dev.

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show abstract

“…Therefore, in mice that are lacking the unfolded protein response‐associated genes, the embryos do not survive beyond pre‐implantation. All of this indicates the important role of these responses in pre‐implantation embryos 35. In addition, the stress response pathways that are linked to Perk activate nuclear factor erythroid 2‐related factor 2 (NRF2).…”

Section: Effect Of Freezing and Thawing In Assisted Reproductive Techmentioning

confidence: 99%

Theory about the Embryo Cryo‐Treatment

Vladimirov

Tacheva

Dı́ez

2017

Reprod Medicine & Biology

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BackgroundTo create hypothesis, which can give a logical explanation related to the benefits of freezing/thawing embryos. Cryopreservation is not only a technology used for storing embryos, but also a method of embryo treatment that can potentially improve the success rate in infertile couples.MethodsFrom the analysis of multiple results in assisted reproductive technology, which have no satisfactory explanation to date, we found evidence to support a ‘therapeutic’ effect of the freezing/thawing of embryos on the process of recovery of the embryo and its subsequent implantation.ResultsFreezing/thawing is a way to activate the endogenous survival and repair responses in preimplantation embryos. Several molecular mechanisms can explain the higher success rate of ET using thawed embryos compared to fresh ET in women of advanced reproductive age, the higher miscarriage rate in cases of thawed blastocyst ET compared to thawed ET at early cleavage embryo, and the higher perinatal parameters of born children after thawed ET. Embryo thawing induces a stress. Controlled stress is not necessarily detrimental, because it generates a phenomenon that is counteracted by several known biological responses aimed to repair mitochondrial damage of membrane and protein misfolding. The term for favorable biological responses to low exposures to stress is called hormesis.ConclusionsThis thesis will summarize the role of cryopreservation in the activation of a hormetic response, preserving the mitochondrial function, improving survival, and having an impact on the process of implantation, miscarriage, and the development of pregnancy.

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Quantitative analysis of mitochondrial RNA in goat–sheep cloned embryos

Yang

Zhang

et al. 2007

Molecular Reproduction Devel

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Mitochondria are the key generators of cellular ATP, and contain extranuclear genome-mitochondrial DNA (mtDNA). In the process of nuclear transfer (NT), heteroplasmic sources of mtDNA from a donor cell and a recipient oocyte are mixed in the cytoplasm of the reconstituted embryo. Previous studies showed inconsistent patterns of mtDNA inheritance in offspring and early fetuses generated through interspecies NT. The quantitative analysis of mitochondrial RNA (mtRNA) in interspecies cloned embryos is useful for better understanding the fate of two types of mitochondria. The components of nicotinamide adenine dinucleotide (NADH) dehydrogenase were coded by both nuclear DNA (nDNA) and mtDNA. The Subunit 1 (ND-1) is one of seven NADH dehydrogenase subunits coded by mtDNA. In present study, using real-time and reverse-transcription PCR, the copy number of species-specific ND-1 mRNA was examined in goat-sheep cloned embryos of various developmental stages, and was applied to evaluate the expression pattern of species-specific mtDNA. The results of showed that (1) the expression of mtDNA derived from goat fetal fibroblast (GFF) decreased from 1-cell stage (immediately after fused) to 2-cell stage, and could not be detected from 4-cell stage onward to blastocyst stage; (2) the expression of mtDNA derived from sheep oocyte was roughly constant from 1-cell stage to the 8-cell stage, increased gradually from 16-cell stage, and sharply at morula and blastocyst stage. Moreover, we strongly argued a mechanism, that is GFF-derived mitochondria were degraded for the depression of bioenergetic functions, and then selectively eliminated during the embryogenesis of goat-sheep cloned embryos.

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Increase of mitochondrial DNA content and transcripts in early bovine embryogenesis associated with upregulation of mtTFA and NRF1 transcription factors

Abstract: Background: Recent work has shown that mitochondrial biogenesis and mitochondrial functions are critical determinants of embryonic development. However, the expression of the factors controlling mitochondrial biogenesis in early embryogenesis has received little attention so far.

Cited by 149 publications

References 39 publications

Maternal age and in vitro culture affect mitochondrial number and function in equine oocytes and embryos

Maternal age and in vitro culture affect mitochondrial number and function in equine oocytes and embryos

Theory about the Embryo Cryo‐Treatment

Quantitative analysis of mitochondrial RNA in goat–sheep cloned embryos

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