Steroid hormones interact with natriuretic peptide C to delay nuclear maturation, to maintain oocyte–cumulus communication and to improve the quality of in vitro-produced embryos in cattle

Abstract

In vivo, oocyte maturation is triggered by the ovulatory LH surge, whereas in vitro it is precociously induced when the cumulus-oocyte complex is removed from the follicle. Natriuretic peptide C (NPPC) delays germinal vesicle breakdown (GVBD) while increasing oocyte-cumulus communication during in vitro maturation (IVM) in cattle. In the present study we first tested the hypothesis that steroids secreted by the follicle (17β-oestradiol, progesterone and androstenedione) interact with NPPC to delay GVBD and to maintain oocyte-cumulus communication as assessed by transfer of a dye (Lucifer Yellow) from the oocyte to cumulus cells. Then, we assessed the effects of steroid hormones and NPPC, alone and in combination in a pre-IVM culture, on embryo production. The combination of NPPC with steroids delayed GVDB, increased natriuretic peptide receptor 2 (NPR2) mRNA abundance in cumulus cells during culture, and maintained oocyte-cumulus communication at levels not different from non-cultured controls. The addition of steroids and/or NPPC to a pre-IVM culture did not alter blastocyst rates after IVF, but supplementation with steroids increased blastocyst total cell number. The present study provides evidence, for the first time in cattle, that steroids interact with NPPC to regulate oocyte nuclear maturation and oocyte-cumulus communication, and improve oocyte developmental competence.

Follicle priming by FSH and pre-maturation culture to improve oocyte quality in vivo and in vitro

“…Cumulus cell-derived cGMP inhibits the reduction of cAMP concentration by the inhibition of PDE3A, an oocyte-specific phosphodiesterase, which is a trigger for meiotic resumption [78]. As with mice, bovine cumulus cells express NPR2 mRNA [65,68,79] and protein [68], and meiotic resumption of oocytes can be arrested during culture of cumulus-oocyte complexes (COCs) with NPPC [65,67,68,70,80]. Although NPR2 was not expressed in oocytes in mice [68], some studies reported the expression of NPR2 mRNA [68,79] and protein [68] in bovine oocyte membranes, and meiotic resumption of denuded oocytes was arrested by NPPC [68].…”

The variable success of in vitro maturation: can we do better?

“…However, in most of the above cited cases the reported results showed only a slight improvement in developmental competence depending on the approach used. Often, rather than increasing the number of blastocysts obtained, an improvement in the parameters related to embryo quality was observed (Luciano et al, 2011;Dieci et al, 2013Dieci et al, , 2016Lodde et al, 2013;Rose et al, 2013;Franciosi et al, 2014;Zeng et al, 2014;Azari-Dolatabad et al, 2016;Li et al, 2016;Park et al, 2016;Sanchez et al, 2017;Soares et al, 2017). For instance, blastocysts with higher number of cells or embryo with better developmental kinetics.…”

Follicular environment and oocyte maturation: roles of local peptides and steroids

“…However, studies using microsurgical removal of the oocyte from the COC and co-culture of oocytectomized COCs with secreting denuded oocytes indicate that OSF are needed for cumulus expansion in mice, but not in cattle, pigs or rats (Buccione et al, 1990;Ralph et al, 1995;Vanderhyden et al, 2003). More recently, the same approach demonstrated that OSF also play a central role in the regulation of glycolytic activity of cumulus cells in mice (Sugiura et al, 2005), whereas in cattle, utilization 602…”

“…Therefore, the enhanced effects on nuclear maturation and gap junction functionality were interpreted as a consequence of greater NPPC signaling and cGMP production in the presence of steroids. Moreover, the combination of NPPC with follicular steroids in a pre-IVM culture promoted improved embryo quality (assessed by total cell number), suggesting that this strategy may be useful to improve IVM/IVF outcomes (Soares et al, 2017).…”