Characterization and Functional Roles of Paternal RNAs in 2-4 Cell Bovine Embryos

Overview

Journal Sci Rep

Specialty Science

Date 2020 Jan 1

PMID 31889064

Citations 12

Authors

Nicole Gross

Maria Giuseppina Strillacci

Francisco Penagaricano

Hasan Khatib

Affiliations

Soon will be listed here.

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.

Citing Articles

Silent cells? Potential for context-dependent gene expression in mature sperm.

Lymbery R, Garcia-Gonzalez F, Evans J Proc Biol Sci. 2025; 292(2038):20241516.

PMID: 39772960 PMC: 11706646. DOI: 10.1098/rspb.2024.1516.

Advanced Skeletal Ossification Is Associated with Genetic Variants in Chronologically Young Beef Heifers.

Shira K, Murdoch B, Davenport K, Becker G, Xie S, Colacchio A Genes (Basel). 2023; 14(8).

PMID: 37628680 PMC: 10454746. DOI: 10.3390/genes14081629.

Pre-Implantation Bovine Embryo Evaluation-From Optics to Omics and Beyond.

Rabel R, Marchioretto P, Bangert E, Wilson K, Milner D, Wheeler M Animals (Basel). 2023; 13(13).

PMID: 37443900 PMC: 10339960. DOI: 10.3390/ani13132102.

The Sperm Small RNA Transcriptome: Implications beyond Reproductive Disorder.

Chan S, Wan C, Law T, Chan D, Fok E Int J Mol Sci. 2022; 23(24).

PMID: 36555356 PMC: 9779749. DOI: 10.3390/ijms232415716.

Identification of differentially expressed mRNAs and miRNAs in spermatozoa of bulls of varying fertility.

Donnellan E, Perrier J, Keogh K, Stiavnicka M, Collins C, Dunleavy E Front Vet Sci. 2022; 9:993561.

PMID: 36277068 PMC: 9581129. DOI: 10.3389/fvets.2022.993561.

References

Haataja L, Kaartinen V, Groffen J, Heisterkamp N . The small GTPase Rac3 interacts with the integrin-binding protein CIB and promotes integrin alpha(IIb)beta(3)-mediated adhesion and spreading. J Biol Chem. 2002; 277(10):8321-8. DOI: 10.1074/jbc.M105363200. View

Goodrich R, Johnson G, Krawetz S . The preparation of human spermatozoal RNA for clinical analysis. Arch Androl. 2007; 53(3):161-7. DOI: 10.1080/01485010701216526. View

Klose R, Bird A . Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci. 2006; 31(2):89-97. DOI: 10.1016/j.tibs.2005.12.008. View

Fang L, Zhou Y, Liu S, Jiang J, Bickhart D, Null D . Integrating Signals from Sperm Methylome Analysis and Genome-Wide Association Study for a Better Understanding of Male Fertility in Cattle. Epigenomes. 2021; 3(2). PMC: 8594688. DOI: 10.3390/epigenomes3020010. View

Kashir J, Nomikos M, Lai F . Phospholipase C zeta and calcium oscillations at fertilisation: The evidence, applications, and further questions. Adv Biol Regul. 2017; 67:148-162. DOI: 10.1016/j.jbior.2017.10.012. View

Gentsch G, Spruce T, Owens N, Smith J . Maternal pluripotency factors initiate extensive chromatin remodelling to predefine first response to inductive signals. Nat Commun. 2019; 10(1):4269. PMC: 6753111. DOI: 10.1038/s41467-019-12263-w. View

Card C, Krieger K, Kaproth M, Sartini B . Oligo-dT selected spermatozoal transcript profiles differ among higher and lower fertility dairy sires. Anim Reprod Sci. 2017; 177:105-123. DOI: 10.1016/j.anireprosci.2016.12.011. View

Boyer A, Girard M, Thimmanahalli D, Levasseur A, Celeste C, Paquet M . mTOR Regulates Gap Junction Alpha-1 Protein Trafficking in Sertoli Cells and Is Required for the Maintenance of Spermatogenesis in Mice. Biol Reprod. 2016; 95(1):13. PMC: 5029431. DOI: 10.1095/biolreprod.115.138016. View

Anders S, Pyl P, Huber W . HTSeq--a Python framework to work with high-throughput sequencing data. Bioinformatics. 2014; 31(2):166-9. PMC: 4287950. DOI: 10.1093/bioinformatics/btu638. View

10.

Kanka J, Nemcova L, Toralova T, Vodickova-Kepkova K, Vodicka P, Jeseta M . Association of the transcription profile of bovine oocytes and embryos with developmental potential. Anim Reprod Sci. 2012; 134(1-2):29-35. DOI: 10.1016/j.anireprosci.2012.08.008. View

11.

Schier A . The maternal-zygotic transition: death and birth of RNAs. Science. 2007; 316(5823):406-7. DOI: 10.1126/science.1140693. View

12.

Sagirkaya H, Misirlioglu M, Kaya A, First N, Parrish J, Memili E . Developmental and molecular correlates of bovine preimplantation embryos. Reproduction. 2006; 131(5):895-904. DOI: 10.1530/rep.1.01021. View

13.

Zhang J, Houston D, King M, Payne C, Wylie C, Heasman J . The role of maternal VegT in establishing the primary germ layers in Xenopus embryos. Cell. 1998; 94(4):515-24. DOI: 10.1016/s0092-8674(00)81592-5. View

14.

Nozawa K, Satouh Y, Fujimoto T, Oji A, Ikawa M . Sperm-borne phospholipase C zeta-1 ensures monospermic fertilization in mice. Sci Rep. 2018; 8(1):1315. PMC: 5778054. DOI: 10.1038/s41598-018-19497-6. View

15.

Cuykendall T, Houston D . Vegetally localized Xenopus trim36 regulates cortical rotation and dorsal axis formation. Development. 2009; 136(18):3057-65. PMC: 2730363. DOI: 10.1242/dev.036855. View

16.

Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A . Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002; 3(7):RESEARCH0034. PMC: 126239. DOI: 10.1186/gb-2002-3-7-research0034. View

17.

Wang H, Wan H, Li X, Liu W, Chen Q, Wang Y . Atg7 is required for acrosome biogenesis during spermatogenesis in mice. Cell Res. 2014; 24(7):852-69. PMC: 4085765. DOI: 10.1038/cr.2014.70. View

18.

Hammond G . Plasma steroid-binding proteins: primary gatekeepers of steroid hormone action. J Endocrinol. 2016; 230(1):R13-25. PMC: 5064763. DOI: 10.1530/JOE-16-0070. View

19.

Wei J, Huang K, Yang C, Kang C . Non-coding RNAs as regulators in epigenetics (Review). Oncol Rep. 2016; 37(1):3-9. DOI: 10.3892/or.2016.5236. View

20.

Huang D, Sherman B, Lempicki R . Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009; 4(1):44-57. DOI: 10.1038/nprot.2008.211. View