Oviduct-Embryo Interactions in Cattle: Two-Way Traffic or a One-Way Street?1

Abstract

This study examined the effect of the presence of single or multiple embryos on the transcriptome of the bovine oviduct. In experiment 1, cyclic (nonbred, n = 6) and pregnant (artificially inseminated, n = 11) heifers were slaughtered on Day 3 after estrus, and the ampulla and isthmic regions of the oviduct ipsilateral to the corpus luteum were separately flushed. Oviductal epithelial cells from the isthmus region, in which all oocytes/embryos were located, were snap-frozen for microarray analysis. In experiment 2, heifers were divided into cyclic (nonbred, n = 6) or pregnant (multiple embryo transfer, n = 10) groups. In vitro-produced presumptive zygotes were transferred endoscopically to the ipsilateral oviduct on Day 1.5 postestrus (n = 50 zygotes/heifer). Heifers were slaughtered on Day 3, and oviductal isthmus epithelial cells were recovered for RNA sequencing. Microarray analysis in experiment 1 failed to detect any difference in the transcriptome of the oviductal isthmus induced by the presence of a single embryo. In experiment 2, following multiple embryo transfer, RNA sequencing revealed 278 differentially expressed genes, of which 123 were up-regulated and 155 were down-regulated in pregnant heifers. Most of the down-regulated genes were related to immune function. In conclusion, the presence of multiple embryos in the oviduct resulted in the detection of differentially expressed genes in the oviductal isthmus; failure to detect changes in the oviduct transcriptome in the presence of a single embryo may be due to the effect being local and undetectable under the conditions of this study.

Role of the oviduct and oviduct-derived products in ruminant embryo development

“…Thus, in pigs Almiñana et al (2012) showed that embryo-maternal communication exists at earliest stages of pregnancy, before the well-known embryonic signal of maternal recognition. In contrast, Maillo et al (2015) did not find differences in the bovine oviduct transcriptome in the presence or absence of an 8-to 16-cell embryo in vivo. Obviously, multi-ovulatory species like mice and pigs cannot be directly compared with mono-ovulatory species such as cattle.…”

“…In a recent study from our group, it was necessary to transfer multiple embryos (up to 50) into the oviducts of heifers to detect differences in the transcriptome. When a single embryo was transferd into the oviduct (pregnant vs cyclic heifers) no differences were found, suggesting a local effect of the embryo (Maillo et al, 2015). More recently, Smits et al (2016) reported a local influence of the embryo on the transcriptome of the equine oviduct epithelium.…”

Spatial differences in gene expression in the bovine oviduct

“…In order to test the effect of region (ampulla vs isthmus), localization relative to the CL (ipsilateral vs contralateral), presence of sperm and presence of an embryo, the following array comparisons were carried out: (Maillo et al 2015); therefore it will not be discussed in this study.…”

“…We have previously described changes in the oviductal transcriptome in pregnant heifers following the transfer of multiple embryos (Maillo et al 2015). There is a paucity of data on the spatial variation on gene expression within the oviduct.…”

Basic and practical aspects of pregnancy establishment in cattle

“…Today, the active role of the oviduct is becoming more and more clear with a growing list of activities both as preparation for an embryo to arrive as well as reactions to its actual presence (Artemenko et al, 2015;GonellaDiaza et al, 2015GonellaDiaza et al, , 2017Maillo et al, 2016b). One challenge for this kind of work seems to be able to detect the changes when they are only caused by a single embryo (Maillo et al, 2015).…”