Zinc deficiency during in vitro maturation of porcine oocytes causes meiotic block and developmental failure

Abstract

The present study investigated the effects of zinc deficiency during in vitro maturation (IVM) of porcine oocytes. Zinc deficiency was induced by administering the membrane‑permeable zinc chelator N,N,N',N'‑tetrakis‑(2‑pyridylmethyl)‑ethylendiamine (TPEN). First, the effects of zinc deficiency during IVM on a TPEN‑treated group and a TPEN+zinc-treated group compared with a control group were assessed. The oocyte maturation rates and subsequent embryonic developmental competence of the TPEN+zinc‑treated oocytes were similar to those of the control oocytes (metaphase II [MII] rate, 93.0 and 92.7%, respectively, and blastocyst [BL] formation rate, 42.0 and 40.0%, respectively). These results were significantly different from those obtained for the TPEN‑treated oocytes (MII rate, 0.61%; BL formation rate, 0%). Although the TPEN‑treated oocytes were arrested at metaphase I (MI), the distribution of microtubules was normal. However, microfilament formation was abnormal in the TPEN‑treated oocytes. Furthermore, the effect of a temporary zinc deficiency during IVM on oocyte maturation and subsequent embryonic development was assessed. TPEN (10 µM) was added to the IVM medium for 0, 7, 15 or 22 h. The 0 h‑treated oocytes showed an 83.9% MII rate, while the 7 h‑treated oocytes had a significantly lower MII rate (44.8%). Most of the 15- and 22 h‑treated oocytes were arrested at MI (MI rate: 98.0 and 97.2%, respectively; MII rate, 0% in both groups). Reductions in the BL formation were dependent on the TPEN treatment duration (29.3, 9.2, 0, and 0% after 0, 7, 15 and 22 h, respectively). In conclusion, zinc is an essential element for successful oocyte maturation and embryonic development in pigs. Zinc deficiency caused a meiotic block and had lasting effects on early embryonic development.

Morphogenesis-related gene-expression profile in porcine oocytes before and after in vitro maturation

“…However, our results identified MAP1B mRNA expression in porcine oocytes before and after IVM. The role of microtubule formation during nuclear and cytoplasmic maturation in mammalian oocytes, particularly in mouse, bovine, and pigs, is well recognized (Chen et al ., 2014; Zhang et al ., 2014; Jeon et al ., 2015; Mahdipour et al ., 2015; Solc et al ., 2015). However, most results are related to the oocyte's cytoskeleton, centrosome, or microtubule modifications during cell cycle progression and chromosome segregation during meiotic oocyte maturation.…”

Zinc supports transcription and improves meiotic competence of growing bovine oocytes

“…In the immature fully grown oocyte, zinc is implicated in the maintenance of meiotic arrest (Kong et al, 2012, Tian andDiaz, 2012). Conversely, during maturation, there is a rise in total zinc content, which is key for successful oocyte maturation (Kim et al, 2010, Tian and Diaz, 2012, Kong et al, 2014, Jeon et al, 2015. In the MII stage oocyte the quota of zinc loosely bound to biomolecules in a readily exchangeable form (Outten andO'Halloran, 2001, Dean et al, 2012), referred to as "labile zinc" or "free zinc", is accumulated in cortical vesicle-like structures that are released in the extracellular compartment upon fertilization through repetitive exocytic events termed "zinc sparks", which are in turn implicated in the process of meiotic resumption and block of polyspermy (Bernhardt et al, 2012, Duncan et al, 2016, Que et al, 2017, Que et al, 2019, Zhao et al, 2014.…”

A role for the transcription factor Mca1 in activating the meiosis-specific copper transporter Mfc1

“…In murine oocytes, zinc insufficiency blocks the exit from meiosis I [ 10 ]. In the case of female porcine gametes, zinc-insufficient oocytes fail to segregate homologous chromosomes, exhibiting an arrest at metaphase I [ 11 ]. Similarly, studies with the yeast S .…”