Preovulatory follicle contributions to oocyte competence in cattle: importance of the ever-evolving intrafollicular environment leading up to the luteinizing hormone surge

Abstract

The preovulatory intrafollicular environment plays a major role in determining oocyte competence. The basis of this review is to highlight the importance of the preovulatory follicle's physiological status prior to the preovulatory luteinizing hormone (LH) surge and onset of oocyte maturation to promote an optimal follicular microenvironment and optimal oocyte developmental competence in cattle. While the underlying mechanisms remain unclear, and are likely multifactorial, the preovulatory follicle's physiological status prior to the preovulatory LH surge is highly influential on the oocyte's capacity to undergo postfertilization embryo development. Changes in the intrafollicular environment of the preovulatory follicle including steroid hormone production, metabolome profiles, and proteome profiles likely support the oocyte's developmental and metabolic competency. This review focuses on the relationship between bovine oocyte developmental competency and antral follicle progression to the preovulatory phase, the role of the preovulatory follicle in improving oocyte developmental competence in cattle, and the importance of the ever-evolving preovulatory intrafollicular environment for optimal fertility.

Keywords: cattle; intrafollicular environment; oocyte competence; preovulatory follicle.

Figure 1.

Schematic depicting the important hormonal and cumulus–oocyte complex changes during proestrus and estrus. After luteolysis, the follicular phase of the estrous cycle begins, starting with proestrus. A decline in progesterone allows for an increase in LH pulsatility and a rise in estradiol both in circulation as well as within the follicle itself. During proestrus, the oocyte is completing critical prematuration developmental processes and is arrested at the germinal vesicle stage. At this time, there is bidirectional communication between the oocyte and cumulus cells allowing for critical metabolic modifications to occur. Once the LH surge occurs, the cross-talk between the oocyte and cumulus cells ceases and maturation to the MII stage begins. The intrafollicular hormone profile changes from predominantly estrogen to progesterone. The preovulatory intrafollicular environment influences oocyte developmental competency and the microenvironment of the periovulatory follicle in which the oocyte matures (Created with Biorender.com).

Figure 2.

Schematic depicting possible antral pool of follicles ranging in size of 3 to 8 mm (predominant) from which cumulus–oocytes are collected for use with in vitro production (IVP) of embryos. Because larger follicles are limited in number and may pose issues with clotting depending on collection approaches, cumulus–oocytes utilized for IVP are largely from a pool of estrogen-active (nondominant) antral follicles that have not been exposed to the preovulatory follicular environment (Created with Biorender.com).

Figure 3.

Schematic depicting the development of multiple dominant follicles after FSH administration (A) for multiple ovulation embryo transfer (MOET) and preovulatory follicle development where the LH surge was pharmacologically induced in animals before they expressed estrus (B). Regarding MOET procedure depicted in (A), super stimulation of the ovary using FSH effectively recruits multiple follicles to grow and attain dominance. Greater levels of circulating estradiol cause the LH surge to occur sooner, thereby shortening the proestrus time period by ~20 h. The cumulus–oocyte complexes resident within said follicles are exposed to a shorter prematuration period which may affect developmental competence (i.e., after fertilization, cleavage, and blastocyst development). Ovulated cumulus–oocyte complexes resulting from hyperstimulation with FSH, have diminished metabolic capacity (Created with Biorender.com). Regarding the preovulatory follicle in (B), in cows that do not exhibit estrus before a fixed timed AI (FTAI), exogenous GnRH administration induces the LH surge prematurely (well before the time when it would have occurred spontaneously if expression of estrus had occurred) thereby shorting the cumulus–oocyte’s prematuration time period. Pharmacological induction of the LH surge has been related to reduced oocyte competence, reduced metabolic capacity of the oocyte, as well as altered follicular fluid composition (Created with Biorender.com).