Uterine influences on embryogenesis and early placentation in the horse revealed by transfer of day 10 embryos to day 3 recipient mares

Abstract

Eight day 10 horse embryos were transferred non-surgically to recipient mares that had ovulated 7 days after the donors. The embryonic vesicle was seen ultrasonographically in all eight recipients, and three out of eight (38%) of the vesicles developed an embryo proper with a beating heart. Conceptus expansion was initially slower than that in control mares but continued until day 22 (recipient day 15). Time of fixation of the vesicle was related to its diameter, rather than uterine stage. Although the embryo proper first appeared ultrasonographically on day 22, as normal, it grew more slowly and the allantois expanded more slowly than that in control mares with normal pregnancies. The development of endometrial cups and their secretion of equine chorionic gonadotropin in the two mares allowed to remain pregnant to O50 days occurred at a conceptus age w7 days later than that in the control mares. The results demonstrated the uniqueness of the horse conceptus in being able to overcome a 7-day asynchrony with the uterus, and also highlighted the overriding influence of the uterine environment on conceptus development in the mare.

Successful transfer of day 10 horse embryos: influence of donor–recipient asynchrony on embryo development

“…Development of the five surviving embryos transferred to recipient mares with a K6 day asynchrony is illustrated in Figs 3a-e and 4e-t. As previously reported for the day 10 embryos transferred to K7 day asynchronous uteri (Wilsher & Allen 2009), embryos transferred to uteri with an asynchrony of K6 days showed significantly delayed development compared to AI-derived or synchronously transferred embryos. For example, the tiny echogenic spot believed to represent the embryo proper was often noted in the ventral quadrant of the vesicle between conceptus days 20 and 24 (recipient days 14 and 18), but this was not seen again until the appearance of a much larger embryo more than 4 days later (Figs 3c-e and 4f-h, j-l and m-p).…”

“…We reported recently on the successful transfer of day 10 horse embryos to K7 days asynchronous recipient mares (Wilsher & Allen 2009), which clearly demonstrated an overriding influence of uterine environment on embryonic growth and early placentation. This paper extends that report and describes the rates of embryo survival following transfer of day 10 embryos to recipients that had ovulated from 9 days after to 4 days before the donor mares and discusses the implication of such asynchronous transfers on embryonic growth and conceptus development.…”

“…Recipient mares with a K9 day asynchrony had a significantly lower mean serum progesterone concentration on the day of transfer compared to all other groups (P!0.05), with the exception of the K7 and C4 day asynchronous recipient groups. Figure 2a shows the mean embryonic vesicle diameters of the control (non-transferred embryos derived from artificial insemination) and transferred embryos that survived until conceptus day 22 (recipient days 15-24), in relation to the level of asynchrony of the recipient A full description of these transfers and the subsequent embryonic growth was reported by Wilsher & Allen (2009).…”

Negative uterine asynchrony retards early equine conceptus development and upregulation of placental imprinted genes

“…As in previous studies, early equine embryos transferred to a severely negatively asynchronous uterus were able to adapt and survive without an obvious reduction in their viability, in as much as they were able to establish pregnancy albeit with an obvious retardation in the rate of development [3,8,29]. Moreover, the delay in development was detectable at the level of the transcriptome in that expression of imprinted genes and DNMTs in yolk-sac membrane of conceptuses recovered from an asynchronous uterus was altered, in most cases this involved a reduction presumed to result from delayed upregulation.…”

“…In ruminants, a comparable up-regulation takes place just before trophoblast interdigitation with the endometrium [35] and, while some imprinted genes are expressed earlier in development in ruminants and pigs (namely the blastocyst stage), monoallelic expression doesn't occur until the time of trophoblast apposition and adhesion to the endometrial epithelium [35,37,38]. Although we didn't investigate the precise timing, by analogy to other species we speculate that monoallelic expression of imprinted genes in equine yolk-sac membrane is delayed until implantation is initiated by the disintegration of the embryonic capsule (days 21e23 of pregnancy) [29,39]. Certainly, by day 33, imprinted genes display a parent-oforigin monoallelic expression in equine trophoblast [23].…”