Transcriptome and Proteome Analysis Revealed Key Pathways Regulating Final Stage of Oocyte Maturation of the Turkey (Meleagris gallopavo).

Mariola Słowińska,Andrzej Ciereszko,Joanna Wiśniewska,Ewa Liszewska,Barbara Bilińska,Krzysztof Kozłowski,Łukasz Paukszto,Jan Jankowski,Laura Pardyak,Jan P Jastrzębski

doi:10.3390/ijms221910589

Abstract

In birds, the zona pellucida (ZP) matrix that surrounds the ovulated oocyte—called the inner perivitelline layer—is involved in sperm–zona interaction and successful fertilization. To identify the important genes and proteins connected with the final step of egg development, next-generation sequencing and two-dimensional electrophoresis, combined with mass spectrometry, were used for the analysis of mature oocytes at the F1 developmental stage. A total of 8161 genes and 228 proteins were annotated. Six subfamilies of genes, with codes ZP, ZP1–4, ZPD, and ZPAX, were identified, with the dominant expression of ZPD. The main expression site for ZP1 was the liver; however, granulosa cells may also participate in local ZP1 secretion. A ubiquitination system was identified in mature oocytes, where ZP1 was found to be the main ubiquitinated protein. Analysis of transcripts classified in estrogen receptor (ESR) signaling indicated the presence of ESR1 and ESR2, as well as a set of estrogen-dependent genes involved in both genomic and nongenomic mechanisms for the regulation of gene expression by estrogen. Oxidative phosphorylation was found to be a possible source of adenosine triphosphate, and the nuclear factor erythroid 2-related factor 2 signaling pathway could be involved in the response against oxidative stress. Oocyte–granulosa cell communication by tight, adherens, and gap junctions seems to be essential for the final step of oocyte maturation.

Highlights

The zona pellucida (ZP) matrix that surrounds the ovulated oocyte—called the inner perivitelline layer (IPVL)—is involved in sperm binding during the initial process of fertilization in birds [1]
The main expression site for ZP1 was found in the liver; granulosa cells (GCs) may partially participate in local ZP1 secretion
Phylogenetic analysis indicated that turkey ZP glycoproteins are conserved among galliforms

Summary

Introduction

The zona pellucida (ZP) matrix that surrounds the ovulated oocyte—called the inner perivitelline layer (IPVL)—is involved in sperm binding during the initial process of fertilization in birds [1]. Fertilization begins from sperm penetration of the IPVL, mostly in the germinal disc region, and it has been suggested that ZP glycoproteins and their turnover, including ZP1 ubiquitination, play a crucial role in sperm–zona interaction [2]. The most dominant ZP glycoproteins of the bird’s mature egg coat (ZP1, ZP3, and ZPD). The GC layer surrounding the bird oocyte plays a key role in the regulation of follicle secretion [12] and in the formation of the IPVL in yellow follicles up to egg ovulation [13] Based on general phylogenetic analysis of vertebrates, chicken ZP glycoprotein genes have been classified into six subfamilies: ZP1, ZP2/ZPA, ZP3/ZPC, ZP4/ZPB, ZPD, and ZPAX [11]; there is lack of comprehensive analyses of ZP genes for other bird species.

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