Abstract
Neurotrophin-4 (NT-4) is a neurotrophic factor that plays an important role in follicular development and oocyte maturation. However, it is not yet known whether NT-4 is related to oocyte maturation and follicular development in pigs. This study aims to investigate the effects of NT-4 supplementation during in vitro maturation (IVM) of porcine oocytes and subsequent embryonic development after parthenogenetic activation (PA). First, NT-4 and its receptors (TrkB and p75NTR) were identified through fluorescent immunohistochemistry in porcine ovaries. NT-4 was mainly expressed in theca and granulosa cells; phospho-TrkB and total TrkB were expressed in theca cells, granulosa cells, and oocytes; p75NTR was expressed in all follicular cells. During IVM, the defined maturation medium was supplemented with various concentrations of NT-4 (0, 1, 10, and 100 ng/mL). After IVM, the nuclear maturation rate was significantly higher in the 10 and 100 ng/mL NT-4 treated groups than in the control. There was no significant difference in the intracellular reactive oxygen species levels in any group after IVM, but the 1 and 10 ng/mL NT-4 treatment groups showed a significant increase in the intracellular glutathione levels compared to the control. In matured cumulus cells, the 10 ng/mL NT-4 treatment group showed significantly increased cumulus expansion-related genes and epidermal growth factor (EGF) signaling pathway-related genes. In matured oocytes, the 10 ng/mL treatment group showed significantly increased expression of cell proliferation-related genes, antioxidant-related genes, and EGF signaling pathway-related genes. We also investigated the subsequent embryonic developmental competence of PA embryos. After PA, the cleavage rates significantly increased in the 10 and 100 ng/mL NT-4 treatment groups. Although there was no significant difference in the total cell number of blastocysts, only the 10 ng/mL NT-4 treatment group showed a higher blastocyst formation rate than the control group. Our findings suggest that supplementation with the 10 ng/mL NT-4 can enhance porcine oocyte maturation by interacting with the EGF receptor signaling pathway. In addition, we demonstrated for the first time that NT-4 is not only required for porcine follicular development, but also has beneficial effects on oocyte maturation and developmental competence of PA embryos.
Highlights
Reproductive biotechnology plays an essential role in understanding the process of transferring genetic information through germ cells to the generation [1, 2]
The mRNA transcripts of NT-4, full-length tropomyosin receptor kinase B (TrkB), truncated TrkB, and p75NTR were detected in all porcine follicular cells containing granulosa cells (GCs), cumulus cell (CC), immature, and matured (MII) oocytes (Figure 1A)
Total TrkB (t-TrkB) was strongly expressed in theca interna cells, theca externa cells, GCs, and CCs (Figure 1C). p75NTR was expressed in all follicular cells (Figure 1D)
Summary
Reproductive biotechnology plays an essential role in understanding the process of transferring genetic information through germ cells to the generation [1, 2]. It is an important growth factor that plays a supporting role in ovarian follicular development and oocyte maturation through its interaction with the high-affinity tropomyosin receptor kinase B (TrkB) and the low-affinity panneurotrophin receptor (p75NTR) [22,23,24]. Both Nt-4 and TrkB mRNAs are expressed in the neonatal rat ovary, and NT-4 can affect early follicular development in rats [17]. BDNF, which binds to TrkB like NT-4, has already been shown to improve mammalian oocyte maturation [25,26,27], but there has been limited research on the relationship between NT-4 and porcine oocyte maturation
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