Reproduction in Domestic Animals

Reprod Dom Anim 43 (Suppl. 2), 393–400 (2008); doi: 10.1111/j.1439-0531.2008.01190.xISSN 0936-6768Factors Affecting Oocyte Quality: Who is Driving the Follicle?P Mermillod, R Dalbie` s-Tran, S Uzbekova, A The´lie, J-M Traverso, C Perreau, P Papillier and P MongetPhysiologie de la Reproduction et des Comportements, UMR 6175 INRA, CNRS, Universite´ de Tours, Haras Nationaux, Nouzilly, FranceContentsMammalian ovaries contain a large stock of oocytes enclosedin primordial follicles. Ovarian cyclic activity induces some ofthese follicles to initiate growth towards a possible ovulation.However, most of these follicles terminate their growth at anymoment and degenerate through atresia. In growing follicles,only a subset of oocytes are capable to support meiosis,fertilization and early embryo development to the blastocyststage, as shown through embryo in vitro production experiments.This proportion of competent oocytes is increasingalong with follicular size. Growing lines of evidence suggestthat oocyte competence relies on the storage of gene products(messenger RNA or protein) that will be determinant tosupport early stages of embryo development, before fullactivation of embryonic genome. Given these facts, thequestion is: are these gene products stored in oocytes duringlate folliculogenesis, allowing an increasing proportion of themto become competent? Alternatively, these transcripts may bestored during early folliculogenesis as the oocyte grows anddisplays high transcription activity. Several arguments supportthis latter hypothesis and are discussed in this review: (i) manyattempts at prolonged culture of oocytes from antral follicleshave failed to increase developmental competence, suggestingthat developmental competence may be acquired before antralformation; (ii) the recent discovery of oocyte secreted factorsand of their ability to regulate many parameters of surroundingsomatic cells, possibly influencing the fate of folliclesbetween ovulation or atresia, suggests a central role of oocytequality in the success of folliculogenesis. Finally, in addition totheir role in interfollicular regulation of ovulation rate, latefolliculogenesis regulation and atresia could also be seen as aselective process aimed at the elimination through follicularatresia of oocytes that did not succeed to store proper geneproducts set during their growth.IntroductionIn mammals, the ovulation delivers a very special cell:the oocyte. This cell has encountered a long andcomplex process of differentiation, leading to thereduction of DNA complement from 2n to n and tothe preparation of the cytoplasm to orchestrate thefusion of the male and female genome complements andthe remodelling of the resulting complete genomecapable to ensure the early development and cell lineagedifferentiation.These particularities place the mammalian oocyte atthe centre of the procreation process. In addition, therecent emergence of embryo-based technologies [in vitrofertilization (IVF), transgenesis and cloning] has reinforcedthe interest of the scientific community into theoocyte. Beyond these applications, the study of oocytefunctions and specificities provides interesting clues forthe better comprehension of several basic biologicalprocesses (cell cycle regulation, genome silencing, posttranscriptionalregulation of gene expression, etc.).The oocyte enters the meiotic division cycle in thefoetal gonad and stops the meiotic progression at thelate prophase stage (diplotene stage, germinal vesicle)around the time of birth, depending on the species. Itremains at this meiotic stage for the complete durationof oocyte growth in the ovarian follicle. During folliculogenesis,the oocyte grows, undergoes modifications ofits ultrastructure and stores the RNA and proteinmaterials necessary to finally become competent toresume and complete maturation, support fertilizationand initiate chromatin remodelling and embryo development.These different competencies are sequentialacquisitions during oocyte differentiation (Sirard et al.2006). The ability to resume meiosis [germinal vesiclebreakdown (GVBD)], to progress to metaphase I and tometaphase II may appear sequentially in some specieslike sheep and goats (Mermillod et al. 1999). In cattle,one can consider that all oocytes are meioticallycompetent soon after antrum formation. Indeed,oocytes from antral follicles spontaneously resumemeiosis when placed in culture (Edwards 1965).At this stage of meiotic competence, not all oocytesare able to be fertilized and to initiate early embryodevelopment. These acquisitions seem to be progressivein the course of follicular growth. It means that theproportion of competent oocytes increases during folliculogenesis,but at the end very few oocytes reach thefinal stage of full competence because of the loss of mostfollicles by physiological atresia occurring at any time oftheir growth. Therefore, the progression of the proportionof competent oocytes within the population ofgrowing follicles may be the result of late oocytedifferentiation through accumulation of factors (messengers,proteins), which will be involved in the successof early developmental steps or the result of the selectionof follicles containing the more fit oocytes, in anincreasingly selective hormonal environment and challenginginterfollicular regulation.The scope of this short review will be to define oocytecompetence, to describe experimental models designedin domestic species for the study of this competence andto discuss respective inputs of oocyte and surroundingsomatic cells in driving an ovarian follicle to ovulationand delivery of a fully competent oocyte.Oocyte Competence Definition and EvaluationDevelopmental competence of the oocyte (or oocytequality) may be defined as its ability to mature, befertilized and give rise to normal and fertile offspringafter normal gestation (Duranthon and Renard 2001).Although the ability of oocytes to reach theblastocyst stage in culture is not a perfect reflection ofÓ 2008 The Authors. 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