Concentration of progesterone during the development of the ovulatory follicle: II. Ovarian and uterine responses

Abstract

Two experiments evaluated the influence of altering the concentrations of progesterone during the development of the ovulatory follicle on the composition of the follicular fluid, circulating LH and PGF(2α) metabolite (PGFM), and expression of endometrial progesterone receptor and estrogen receptor-α. In both experiments, the estrous cycles were presynchronized (GnRH and progesterone insert followed by insert removal and PGF(2α) 7 d later, and GnRH after 48 h) and cows were then enrolled in 1 of 2 treatments 7 d later (study d -16): high progesterone (HP) or low progesterone (LP). In experiment 1 (n=19), cows had their estrous cycle synchronized starting on study d -9 (GnRH and progesterone insert on d -9, and insert removal and PGF(2α) on d -2). In experiment 2 (n=25), cows were submitted to the same synchronization protocol as in experiment 1, but had ovulation induced with GnRH on study d 0. In experiment 1, plasma was sampled on d -4 and analyzed for concentrations of LH; the dominant follicle was aspirated on d 0 and the fluid analyzed for concentrations of progesterone, estradiol, and free and total IGF-1. In experiment 2, follicular development and concentrations of progesterone and estradiol in plasma were evaluated until study d 16. Uterine biopsies were collected on d 12 and 16 for progesterone receptor and estrogen receptor-α protein abundance. An estradiol/oxytocin challenge for PGFM measurements in plasma was performed on d 16. In experiments 1 and 2, LP cows had lower plasma concentrations of progesterone and greater concentrations of estradiol, and had larger ovulatory follicle diameter (20.4 vs. 17.2mm) at the end of the synchronization protocol than HP cows. Concentration of LH tended to be greater for LP than HP cows (0.98 vs. 0.84 ng/mL). The dominant follicle of LP cows had greater concentration of estradiol (387.5 vs. 330.9 ng/mL) and a lower concentration of total IGF-1 (40.9 vs. 51.7 ng/mL) than that of HP cows. In experiment 2, estradiol and progesterone concentrations did not differ between treatments from d 0 to 16; however, the proportion of cows with a short luteal phase tended to increase in LP than HP (25 vs. 0%). Concentrations of PGFM were greater for LP than HP. Uterine biopsies had a greater abundance of progesterone receptor, and tended to have less estrogen receptor-α abundance on d 12 compared with d 16. An interaction between treatment and day of collection was detected for estrogen receptor-α because of an earlier increase in protein abundance on d 12. Reduced concentrations of progesterone during the development of the ovulatory follicle altered follicular dynamics and follicular fluid composition, increased basal LH concentrations, and prematurely increased estrogen receptor-α abundance and exacerbated PGF(2α) release in the subsequent estrous cycle.

Physiological and practical effects of progesterone on reproduction in dairy cattle

“…However, a recent study that flushed embryos from single ovulating cows that had follicles grow during low or high P4 did not find a difference in embryo quality on day 7 (58.3% v. 53.3%) (Cerri et al, 2011a). A companion study (Cerri et al, 2011b) indicated that although cows with low P4 had increased basal LH concentrations and altered follicular dynamics and follicular fluid composition that could alter oocyte quality, a particularly distinct difference in cows with low P4 was the premature development of pathways leading to uterine PGF2α secretion. Thus, altered uterine function could also have an important role in reducing fertility in cows that have low P4 concentrations before AI.…”

Aspects and mechanisms of low fertility in anovulatory dairy cows

“…Fertility of estrous cyclic and anovular lactating dairy cows induced to ovulate the first-wave dominant follicle is usually compromised (Bisinotto et al, 2010). Our work has clearly demonstrated that first-wave follicles that develop concurrently with the CL and, therefore, under low concentrations of progesterone result in alterations in the follicular fluid composition (Cerri et al, 2011a), alterations in endometrial function (Cerri et al, 2011a), reduced embryo quality (Rivera et al, 2011;Wiltbank et al, 2011), and compromised P/AI (Bisinotto et al, 2010). More importantly, our work has shown that progesteron is likely to mediated these changes in reproductive responses of cows ovulating the dominant follicle of the first follicular wave (Bisinotto et al, 2013).…”

“…It is well established that progesterone in the preceding estrous cycle influences endometrial function in the subsequent cycle (Shaham-Albalancy et al ., 1997, 2001). Cows that develop the ovulatory follicle under low concentrations of progesterone have an earlier upregulation of endometrial expression of estrogen receptor-α protein in the postovulatory period and produce more PGF2α following an oxytocin challenge than cows that develop the ovulatory follicle under high concentrations of progesterone (Cerri et al, 2011a). In fact, these cows are more likely to suffer from short luteal phases (Cerri et al, 2011a), which is devastating to maintenance of pregnancy in cattle.…”

“…Progesterone exerts a regulatory effect on the hypothalamus-pituitary-gonadal axis (Clarke and Pompolo, 2005) and differences in progesterone concentrations in plasma affect follicular fluid composition (Cerri et al, 2011a), cumulus expansion and oocyte competence (Fair and Lonergan, 2012), embryo quality (Rivera et al, 2011), and uterine function during the subsequent estrous cycle (ShahamAlbalancy et al, 1997(ShahamAlbalancy et al, , 2001Cerri et al, 2011a). It has been estimated that the CL of dairy cows produce large quantities of progesterone (Wiltbank et al, 2012a), but extensive catabolism by splanchnic tissues in highproducing cows results in concentrations in blood that are often considered inadequate for optimum reproduction (Wiltbank et al, 2006).…”

Progesterone-based fixed-time artificial insemination protocols for dairy cows

“…Several researchers have reported the importance of adequate concentrations of P4 during preovulatory follicle development, particularly in FTAI programs (BILBY et al, 2013;CERRI et al, 2011aCERRI et al, , 2011bCHEBEL et al, 2010;DISKIN et al, 2006;STEVENSON et al, 2006STEVENSON et al, , 2008. Depending on circulating P4 concentrations, the pattern of follicle development can be modified, and low circulating P4 during the growth of the ovulatory follicle is often associated with lower fertility in lactating dairy cows undergoing a FTAI protocol (CERRI et al, 2011a).…”