Preimplantation development in ungulates: a ‘ménage à quatre’ scenario

Abstract

In ungulates, early embryonic development differs dramatically from that of mice and humans and is characterized by an extended period of pre- and peri-implantation development in utero. After hatching from the zona pellucida, the ungulate blastocyst will stay free in the uterus for many days before implanting within the uterine wall. During this protracted peri-implantation period, an intimate dialog between the embryo and the uterus is established through a complex series of paracrine signals. The blastocyst elongates, leading to extreme growth of extra-embryonic tissues, and at the same time, the inner cell mass moves up into the trophoblast and evolves into the embryonic disc, which is directly exposed to molecules present in the uterine fluids. In the peri-implantation period, uterine glands secrete a wide range of molecules, including enzymes, growth factors, adhesion proteins, cytokines, hormones, and nutrients like amino and fatty acids, which are collectively referred to as histotroph. The identification, role, and effects of these secretions on the biology of the conceptus are still being described; however, the studies that have been conducted to date have demonstrated that histotroph is essential for embryonic development and serves a critical function during the pre- and peri implantation periods. Here, we present an overview of current knowledge on the molecular dialogue among embryonic, extraembryonic, and maternal tissues prior to implantation. Taken together, the body of work described here demonstrates the extent to which this dialog enables the coordination of the development of the conceptus with respect to the establishment of embryonic and extra-embryonic tissues as well as in preparation for implantation.

Nicotinamide Supplementation during the In Vitro Maturation of Oocytes Improves the Developmental Competence of Preimplantation Embryos: Potential Link to SIRT1/AKT Signaling

“…Due to the importance of hatching for successful implantation and pregnancy [28,29], we moved forward to delineate the possible mechanisms behind the improved hatching witnessed following NAM treatment. Previously, supplementation of IVM medium with the SIRT1 activator resveratrol improved the quality and the hatching of blastocysts [3].…”

“…At late stages of preimplantation embryo development, blastocysts comprising the two distinct parts, the outer trophectoderm (TE) and the inner cell mass (ICM), tend to hatch out of the zona pellucida. This precisely regulated process, the hatching, is crucial for survival, normal development, and implantation of embryos [ 28 , 29 ]. The critical roles of SIRT1 and AKT signaling in controlling the hatching process were reported [ 3 , 22 , 30 ].…”

Lineage Differentiation Markers as a Proxy for Embryo Viability in Farm Ungulates

“…During the first cell divisions, the embryo relies on maternal transcripts and proteins until the embryonic genome is activated between the 2- (rodents) and 4/8-cell stages (lagomorphs, ungulates, and primates) ( 8 ). At these early stages of development, blastomeres are morphologically indistinguishable, but from the 8-cell stage in the mouse, cells located in the outside of the embryo undergo a process of polarization that will influence their fate, biasing outer polar cells toward trophectoderm (TE) and inner apolar cells toward inner cell mass (ICM) ( 9 – 11 ) ( Figure 1 ). The formation of an apical domain in the outer cells triggers a transcriptional network involving Hippo/YAP signaling and the activation of Tead4 in the mouse, which leads to the downregulation of the pluripotency factor Sox2 and the upregulation of Cdx2 from the morula stage ( 12 – 15 ).…”

β-Lactoglobulin and Glycodelin: Two Sides of the Same Coin?

“…However, both p19 and SAL1 are glycosylated. In all of these animals, and ungulates in general, there is a significant delay before implantation during which the uterine secretions supply a wide range of molecules for nutrition, protection and development ( Artus et al, 2020 ). RBP has also been identified in cat conceptus ( Thatcher et al, 1991 ) and dog endometrium ( Buhi et al, 1995 ).…”