Characterization and functional roles of paternal RNAs in 2-4 cell bovine embryos

Sci Rep. 2019 Dec 30;9(1):20347. doi: 10.1038/s41598-019-55868-3.

Abstract

Embryos utilize oocyte-donated RNAs until they become capable of producing RNAs through embryonic genome activation (EGA). The sperm's influence over pre-EGA RNA content of embryos remains unknown. Recent studies have revealed that sperm donate non-genomic components upon fertilization. Thus, sperm may also contribute to RNA presence in pre-EGA embryos. The first objective of this study was to investigate whether male fertility status is associated with the RNAs present in the bovine embryo prior to EGA. A total of 65 RNAs were found to be differentially expressed between 2-4 cell bovine embryos derived from high and low fertility sires. Expression patterns were confirmed for protein phosphatase 1 regulatory subunit 36 (PPP1R36) and ataxin 2 like (ATXN2L) in three new biological replicates. The knockdown of ATXN2L led to a 22.9% increase in blastocyst development. The second objective of this study was to characterize the parental origin of RNAs present in pre-EGA embryos. Results revealed 472 sperm-derived RNAs, 2575 oocyte-derived RNAs, 2675 RNAs derived from both sperm and oocytes, and 663 embryo-exclusive RNAs. This study uncovers an association of male fertility with developmentally impactful RNAs in 2-4 cell embryos. This study also provides an initial characterization of paternally-contributed RNAs to pre-EGA embryos. Furthermore, a subset of 2-4 cell embryo-specific RNAs was identified.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biomarkers
  • Blastocyst / cytology
  • Blastocyst / metabolism*
  • Cattle
  • Embryo, Mammalian*
  • Embryonic Development / genetics*
  • Female
  • Fertility / genetics
  • Gene Expression Profiling
  • Gene Expression Regulation, Developmental
  • Gene Knockdown Techniques
  • Male
  • Oocytes / metabolism
  • Paternal Inheritance*
  • RNA / genetics*
  • Spermatozoa / metabolism
  • Transcriptome

Substances

  • Biomarkers
  • RNA