Abstract
Thousands of circular RNAs (circRNAs) have been recently discovered in cumulus cells and oocytes from several species. However, the expression and function of circRNA during porcine oocyte meiotic maturation have been never examined. Here, we separately identified 7,067 and 637 circRNAs in both cumulus cells and oocytes via deep sequencing and bioinformatic analysis. Further analysis revealed that a faction of circRNAs is differentially expressed (DE) in a developmental stage-specific manner. The host genes of DE circRNAs are markedly enriched to multiple signaling pathways associated with cumulus cell function and oocyte maturation. Additionally, most DE circRNAs harbor several miRNA targets, suggesting that these DE circRNAs potentially act as miRNA sponge. Importantly, we found that maternal circARMC4 knockdown by siRNA microinjection caused a severely impaired chromosome alignment, and significantly inhibited first polar body extrusion and early embryo development. Taken together, these results demonstrate for the first time that circRNAs are abundantly and dynamically expressed in a developmental stage-specific manner in cumulus cells and oocytes, and maternally expressed circARMC4 is essential for porcine oocyte meiotic maturation and early embryo development.
Highlights
Oocyte meiotic maturation is the last stage of oogenesis and is the indispensable prerequisite for fertilization, preimplantation development of the embryo and even term development [1]
We identified specific circular RNA (circRNA) expressed in oocytes by comparing circRNA transcripts of pure cumulus cells and mixture samples of cumulus cells and oocytes before and after maturation (Figure 1A)
We further showed that circARMC4, a top up-regulated circRNA in oocytes, is required for porcine oocyte meiotic maturation and early embryo development
Summary
Oocyte meiotic maturation is the last stage of oogenesis and is the indispensable prerequisite for fertilization, preimplantation development of the embryo and even term development [1]. Many efforts have been made to improve the oocyte maturation in vitro in pigs, its meiotic and developmental capacity is still suboptimal relative to that under the physiological states [5, 6]. This may be due to the imperfectness of in vitro culture conditions currently used that cannot achieve the optimal maturational outcomes, and there is inadequate information regarding the unique molecular mechanisms of porcine oocyte meiotic maturation [7, 8]. The expression of circRNAs in porcine multiple tissues has been reported [18, 36], its expression and function in porcine oocyte meiotic maturation remain unclear
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