Maternal control of early embryogenesis in mammals

Abstract

Oocyte quality is a critical factor limiting the efficiency of assisted reproductive technologies (ART) and pregnancy success in farm animals and humans. ART success is diminished with increased maternal age, suggesting a close link between poor oocyte quality and ovarian-aging. However, the regulation of oocyte quality remains poorly understood. Oocyte quality is functionally linked to ART success because the maternal-to-embryonic transition is dependent on stored maternal factors, which are accumulated in oocytes during oocyte development and growth. The maternal-to-embryonic transition consists of critical developmental processes including maternal RNA depletion and embryonic genome activation. In recent years, key maternal proteins encoded by maternal-effect genes have been determined, primarily using genetically modified mouse models. These proteins are implicated in various aspects of early embryonic development including maternal mRNA degradation, epigenetic reprogramming, signal transduction, protein translation and initiation of embryonic genome activation. Species differences exist in number of cell divisions encompassing the maternal-to-embryonic transition and maternal-effect genes controlling this developmental window. Perturbations of maternal control result in decreased oocyte quality, some of which are associated with ovarian aging.

Parental contributions to early embryo development: influences of urinary phthalate and phthalate alternatives among couples undergoing IVF treatment

“…Our observed associations with blastocysts, but not cleavage stage embryos, coincides with the timing of the embryonic genome activation (EGA). At the four-to eight-cell stage, corresponding to Day 3 of human embryo development (Niakan et al, 2012), the human embryos are in a stage of relative transcriptional silence, relying on maternally derived products for the first cell divisions (Baroux et al, 2008;Zhang and Smith, 2015). EGA facilitates a transition from maternal to embryonic control, which includes the degradation of maternal mRNAs and major changes in expression of histone isoforms, histone modifications, chromatin structure (Latham and Schultz, 2001) and DNA methylation (Messerschmidt et al, 2014).…”

Evidence Supporting a Role for SMAD2/3 in Bovine Early Embryonic Development: Potential Implications for Embryotropic Actions of Follistatin1

“…Of particular note, during this developmental window, the oocyte accumulates maternal factors, including mRNAs, proteins and energy substrates, which are necessary to foster early embryonic development immediately after fertilization given that early embryos lack transcriptional ability necessary for development until embryonic genome activation (EGA) occurs at 8-to 16-cell stage in cattle and 2-cell stage in mouse [6,7]. Hence, multiple oocyte-stored factors (maternal factors) are required for early embryonic development [7,8]. Such genes, whose deficiency in oocytes results in phenotypes in embryos after fertilization, are classified as maternal-effect genes [7].…”

SMC5/6 is required for the formation of segregation-competent bivalent chromosomes during meiosis I in mouse oocytes

“…These maternal proteins are encoded by maternal-effect genes (Li et al, 2010). Approximately, 45-50 maternal-effect genes have been identified in mammals, and many of these are involved in chromatin structure, modification and genome integrity (Zhang and Smith, 2015). Reduced levels of maternal-effect genes have been associated with the reduced oocyte developmental competence that is characteristic of ovarian aging (Guglielmino et al, 2011;Hamatani et al, 2004;Pan et al, 2008;Zhang and Smith, 2015).…”

“…Approximately, 45-50 maternal-effect genes have been identified in mammals, and many of these are involved in chromatin structure, modification and genome integrity (Zhang and Smith, 2015). Reduced levels of maternal-effect genes have been associated with the reduced oocyte developmental competence that is characteristic of ovarian aging (Guglielmino et al, 2011;Hamatani et al, 2004;Pan et al, 2008;Zhang and Smith, 2015). The IVF experiments presented in this study show that embryogenesis is aberrant only when Smc5 is mutated during the oocyte growth phase, and provision of a functional Smc5 gene from sperm is insufficient to facilitate embryogenesis.…”