Morphologic, Steroidogenic, and Transcriptomic Assessment of the Corpus Luteum in Holstein Cows after Spontaneous or Hormone-Induced Ovulation

SIMPLE SUMMARY: Poor reproductive efficiency in dairy cows is common due to low estrus detection, suboptimal fertility, and high embryonic losses. Synchronized ovulation protocols eliminate estrus detection and enable timed insemination. Refining such protocols for optimal outcomes is an ongoing endeavor. We previously reported that using a porcine luteinizing hormone in lieu of a gonadotropin-releasing hormone to synchronize ovulation significantly increased pregnancy per artificial insemination (AI) and altered intrafollicular protein milieu without affecting the blood concentrations of progesterone, a hormone essential for pregnancy maintenance in cattle. To elucidate underlying mechanisms, we compared the structure and function of corpora lutea that developed spontaneously or after hormone-induced ovulation in Holstein cows. Despite no differences in structure or gene expression, progesterone production by luteal explants was greater after ovulation induced with the porcine luteinizing hormone compared to other treatments. We inferred that augmented ovarian-level progesterone production likely increased uterine-level progesterone concentrations, which could promote embryo development and consequently increase pregnancy per AI. ABSTRACT: There is evidence that replacing the gonadotropin-releasing hormone (GnRH) with porcine luteinizing hormone (pLH) to synchronize ovulation prior to artificial insemination (AI) increased pregnancy per AI in dairy cows without affecting blood progesterone (P(4)) concentrations. Whether morphologic, steroidogenic, and transcriptomic differences exist among corpora lutea (CL) formed after ovulation induced by GnRH and pLH is unclear. Our main objective, therefore, was to compare CL characteristics between GnRH- and pLH-induced CL. In 24 non-lactating Holstein cows, ovulations were spontaneous (Spont-Ov) or induced with 100 µg GnRH, 25 mg pLH, or 1 mg estradiol benzoate (EB), with CL excised 12 d after ovulation. In pLH- versus GnRH-treated cows, the duration of elevated LH (above baseline) was prolonged (10 versus 6 h, respectively, p < 0.01), but CL dimensions, pixel intensity of CL images, proportions of steroidogenic and non-steroidogenic luteal cells, and mean plasma LH did not significantly differ. Post-ovulation mean plasma P(4) (ng/mL) did not differ among Spont-Ov (3.0) pLH (3.1) or GnRH (3.0) cows but were lower in EB cows (2.0). In vitro P(4) concentration was greater in luteal explants of pLH-treated cows than in all other groups (combined means, 16.0 vs. 12.3 µg/mL, p < 0.02). Relative abundance of mRNA for oxytocin receptor (OXTR) was 2-fold higher (p < 0.01) in CL of pLH vs. GnRH cows and highest in Spont-Ov CL. In summary, pLH-treated cows had a longer LH peak, and greatest luteal tissue concentrations and in vitro production of P(4). We inferred that increased P(4) concentrations at the ovarian–uterine level in pLH-treated cows could have promoted embryo development and increased pregnancy per AI.