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Embryo and Its Mitochondria

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Embryo and Its Mitochondria antioxidants Review Embryo and Its Mitochondria Pascale May-Panloup 1,2,* , Magalie Boguenet 2 , Hady El Hachem 3 , Pierre-Emmanuel Bouet 4 and Pascal Reynier 2,5 1 Reproductive Biology Unit, Angers University Hospital, 49000 Angers, France 2 MITOVASC, Angers University, INSERM 1083-CNRS 6015, IBS–CHU, 49000 Angers, France; [email protected] (M.B.); [email protected] (P.R.) 3 Department of Reproductive Medicine, Saint Joseph Fertility Center, Beirut 1100, Lebanon; [email protected] 4 Department of Reproductive Medicine, Angers University Hospital, 49000 Angers, France; [email protected] 5 Department of Biochemistry and Genetics, Angers University Hospital, 49000 Angers, France * Correspondence: [email protected]; Tel.: +33-2-41-35-45-94 Abstract: The mitochondria, present in almost all eukaryotic cells, produce energy but also contribute to many other essential cellular functions. One of the unique characteristics of the mitochondria is that they have their own genome, which is only maternally transmitted via highly specific mech- anisms that occur during gametogenesis and embryogenesis. The mature oocyte has the highest mitochondrial DNA copy number of any cell. This high mitochondrial mass is directly correlated to the capacity of the oocyte to support the early stages of embryo development in many species. Indeed, the subtle energetic and metabolic modifications that are necessary for each of the key steps of early embryonic development rely heavily on the oocyte’s mitochondrial load and activity. For example, epigenetic reprogramming depends on the metabolic cofactors produced by the mitochon- drial metabolism, and the reactive oxygen species derived from the mitochondrial respiratory chain are essential for the regulation of cell signaling in the embryo. All these elements have also led scientists to consider the mitochondria as a potential biomarker of oocyte competence and embryo Citation: May-Panloup, P.; Boguenet, viability, as well as a key target for future potential therapies. However, more studies are needed to M.; El Hachem, H.; Bouet, P.-E.; confirm these findings. This review article summarizes the past two decades of research that have Reynier, P. Embryo and Its led to the current understanding of mitochondrial functions in reproduction Mitochondria. Antioxidants 2021, 10, 139. https://doi.org/10.3390/ Keywords: embryo; mitochondria; mitochondrial DNA antiox10020139 Received: 9 January 2021 Accepted: 18 January 2021 1. Introduction Published: 20 January 2021 The mitochondria are small organelles found in all eukaryotic cells and are thought Publisher’s Note: MDPI stays neutral to have evolved from the endosymbiosis between an ancestral eukaryotic cell and an α- with regard to jurisdictional claims in proteobacteria capable of metabolizing oxygen [1]. They are responsible for the production published maps and institutional affil- of more than 90% of the ATP necessary for cellular function via oxidative phosphorylation iations. (OXPHOS) (Figure1). OXPHOS uses five large multi-enzymatic complexes found in the cristae of the inner mitochondrial membrane: complexes I to IV that constitute the electron transport chain (ETC), and complex V (ATP synthase), which allows synthesizing ATP by phosphorylation using the energy generated by the translocation of protons across Copyright: © 2021 by the authors. the inner membrane. OXPHOS functioning produces most of the endogenous reactive Licensee MDPI, Basel, Switzerland. oxygen species (ROS), which are implicated in many cellular regulation pathways but This article is an open access article could become toxic when they accumulate. Besides their crucial role in energy production, distributed under the terms and mitochondria play an essential role in the biosynthesis of organic compounds, apoptosis, conditions of the Creative Commons calcium homeostasis, and thermogenesis, as well as cellular signal pathways and gene Attribution (CC BY) license (https:// expression [2–4]. creativecommons.org/licenses/by/ 4.0/). Antioxidants 2021, 10, 139. https://doi.org/10.3390/antiox10020139 https://www.mdpi.com/journal/antioxidants Antioxidants 2020, 9, x FOR PEER REVIEW 2 of 20 (DRP1), optic atrophy protein 1 (OPA1), and mitofusins 1 and 2 (MFN1 and MFN2)) found in the mitochondrial membrane. Because of this network, it is often difficult to determine the total number of mitochondria, and the mitochondrial mass is indirectly estimated by quantifying the mitochondrial DNA (mtDNA). Indeed, mitochondria have their own genome, a small (about 16 Kilobases) circular double-stranded DNA [6]. MtDNA contains mostly coding regions that encode 13 subunits of the complexes in- volved in the respiratory chain, 2 rRNAs, and 22 tRNAs. The other mitochondrial pro- teins, estimated to be around 1500, are coded by the nuclear genome and later imported into the mitochondria. The regulation of mitochondrial biogenesis is central to mitochondrial functions. It is engineered, in coordination with the general cell metabolism, by PGC1α (PPAR gamma coactivator 1) and NAD-dependent deacetylases of the sirtuin family. PGC1α is a tran- scription coregulator that controls the activity of transcription factors that activate nu- clear genes involved in β oxidation, antioxidant defense, and the citric acid cycle (Krebs cycle). It also promotes the expression of NRF 1 and 2 (nuclear respiratory factors 1 and 2), which are transcription factors for nuclear genes coding for proteins involved in mi- tochondrial import, in assembly, and complexes of the respiratory chain, as well as fac- tors involved in translation (tRNA and rRNA), transcription, and replication of the mtDNA, such as TFAM (mitochondrial transcription factor A) and POLG (polymerase Antioxidants 2021, 10, 139 gamma), thus allowing the coordination between the nuclear and mitochondrial2 ge- of 19 nomes [7,8]. FigureFigure 1. 1. TheThe mitochondria mitochondria play play a acentral central rol rolee in in energy energy production production by by ATP ATP synthesis synthesis via via oxidative oxidative phosphorylationphosphorylation (OXPHOS). (OXPHOS). OXPHOS OXPHOS uses uses four four large large multi multi-enzymatic-enzymatic complexes complexes (complexes (complexes I to I to IV)IV),, which which constitute constitute the the electron electron transport transport chain, chain, and and complex complex V V,, which synthe synthesizessizes ATP. OXPHOS •− ●− OXPHOSactivity generates activity gener the vastates majoritythe vast ofmajority reactive of oxygenreactive species oxygen (ROS) species (O 2(ROS)). (O2 ). 2. Mitochondria,Each somatic Gametogenesis cell contains hundreds, and mtDNA of mitochondria Transmission that form a dynamic network capable of movement, fusion, and fission, depending on the cellular energy require- For most organisms, maternal uniparental inheritance is the norm, as the mito- ments [5]. These mitochondrial dynamics are mediated by GTPases (dynamin-related chondrial genome is inherited exclusively from the oocyte (Figure 2) [9]. This is the con- protein 1 (DRP1), optic atrophy protein 1 (OPA1), and mitofusins 1 and 2 (MFN1 and sequence of two major events: first of all, paternal mtDNA is eliminated via several MFN2)) found in the mitochondrial membrane. Because of this network, it is often difficult mechanisms: a drastic decrease in the number of mitochondria during spermatogenesis to determine the total number of mitochondria, and the mitochondrial mass is indirectly and an active destruction of mitochondria and/or paternal mtDNA during early embry- estimated by quantifying the mitochondrial DNA (mtDNA). Indeed, mitochondria have ogenesis [10,11]. On the other hand, there is global amplification of the mitochondrial their own genome, a small (about 16 Kilobases) circular double-stranded DNA [6]. MtDNA pool during oogenesis, producing several hundred thousands of copies of mtDNA, contains mostly coding regions that encode 13 subunits of the complexes involved in the making the mature oocyte the cell with the highest number of mitochondria in the or- respiratory chain, 2 rRNAs, and 22 tRNAs. The other mitochondrial proteins, estimated to ganism,be around in all 1500, species are coded [12]. byIn the nuclearhuman genomeoocyte, andthe mean later imported number of into copies the mitochondria. of mtDNA has beenThe estimated regulation to ofbe mitochondrialaround 250,000 biogenesis [13]. is central to mitochondrial functions. It isStudies engineered, on mtDNA in coordination segregation with in anim theal general and human cell metabolism, pedigrees affected by PGC1 by αmtDNA(PPAR mutationsgamma coactivator have shown 1) andthat NAD-dependent, when point mutations deacetylases occur of, thethere sirtuin may family.be a high PGC1-levelα is switchinga transcription of mutants coregulator within thata single controls generation the activity [14–18 of]. transcription This concept factorshas led that to the activate bot- nuclear genes involved in β oxidation, antioxidant defense, and the citric acid cycle (Krebs cycle). It also promotes the expression of NRF 1 and 2 (nuclear respiratory factors 1 and 2), which are transcription factors for nuclear genes coding for proteins involved in mitochondrial import, in assembly, and complexes of the respiratory chain, as well as factors involved in translation (tRNA and rRNA), transcription, and replication of the mtDNA, such as TFAM (mitochondrial transcription factor A) and POLG (polymerase gamma), thus allowing the coordination between the nuclear
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