Elsevier

Theriogenology

Volume 78, Issue 5, 15 September 2012, Pages 1030-1039
Theriogenology

Research article
Effect of purified llama ovulation-inducing factor (OIF) on ovarian function in cattle

https://doi.org/10.1016/j.theriogenology.2012.03.036Get rights and content

Abstract

Two experiments were designed to determine the effect of purified ovulation inducing factor (OIF) on ovarian function in cattle. In Experiment 1, prepubertal heifers (n = 11 per group) were treated on Day 5 (Day 0 = day of follicular wave emergence) of the follicular wave with an intramuscular dose of saline (1 mL), GnRH (100 μg), or purified OIF (1 mg/100 kg body weight). Ovulation occurred in 9/11 heifers treated with GnRH, and 1/11 heifers in each of the OIF- and saline-treated groups (P < 0.05). Compared to saline-treated controls, OIF treatment was associated with a smaller dominant follicle diameter (P < 0.01), a rise in plasma FSH concentration (P < 0.1), and earlier emergence of the next follicular wave (P < 0.05). In Experiment 2, sexually mature heifers were given either GnRH or purified OIF on Days 3, 6 or 9 of the first follicular wave (i.e., early growing, early static, or late static phase of the dominant follicle; n = 5 per group per day), or were untreated (n = 10). In heifers treated with OIF on Day 6, the dominant follicle diameter profile tended to be smaller than in controls, and was associated with a rise (P < 0.05) in plasma FSH concentrations. A similar rise in FSH was detected after OIF treatment on Day 9. Compared to untreated controls, treatment with OIF and GnRH was associated with a larger CL diameter (Days 3 and 6 groups; P < 0.05) and a greater concentration of plasma progesterone (Days 6 and 9 groups; P < 0.05). Treatment with purified OIF did not induce ovulation in heifers, but hastened new follicular wave emergence in prepubertal heifers, influenced follicular dynamics in a phase-specific manner in mature heifers, and was luteotrophic.

Introduction

Spontaneous ovulators, such as cattle, are species capable of ovulating without copulatory stimulation. In the presence of low plasma progesterone concentrations, estradiol secreted by the preovulatory follicle has a positive feedback effect on the hypothalamus, leading to a surge release of LH [1] and initiation of the ovulatory cascade [2]. Conversely, induced ovulators, such as llamas, alpacas and camels, are species that, in the absence of copulation, will not ovulate or do so at a very low incidence (e.g., 5% in alpacas [3], [4], [5]). Although the role of seminal plasma in the induction of ovulation has been examined in some induced ovulators [6], [7], [8], [9], [10], [11], few reports were found regarding the influence of seminal plasma on ovulation in spontaneously ovulating species. In pigs, intrauterine administration of seminal plasma was associated with a reduction in the interval between the LH peak and ovulation [12]. Although no effect on ovulation was detected in another study in pigs [13], administration of seminal plasma was associated with an increase in CL size and progesterone secretion in vivo, and increased LH responsiveness and progesterone secretion of granulosa and theca cells from preovulatory follicles in vitro. No references were found to studies of the effect of seminal plasma on ovulation in cattle.

Results of recent studies on the effects of bovine, equine, and porcine seminal plasma on ovulation in llamas suggest that an ovulation-inducing factor (OIF) may be widely conserved among induced and spontaneous ovulators [14], [15]. After intramuscular treatment with an equivalent volume of seminal plasma from llamas, alpacas and bulls (i.e., 1 mL), ovulation was induced in 19/19 (100%), 19/19 (100%) and 5/19 (26%) female llamas, respectively, all of which were significantly more frequent than in the control group 0/19 (0% [14]). In an earlier study on Bactrian camels, 3/5 females ovulated after intrauterine or intramuscular treatment with bovine seminal plasma [8].

In both llamas and camels, the ovulation-inducing effect of seminal plasma was attributed to a surge release of LH from the pituitary [6], [7], [14], [16]. Further, results of a recent dose–response study in llamas were consistent with the hypothesis that OIF affects ovulation and CL function in a dose-dependent manner, at physiologically relevant doses, i.e., 1/25 to 1/100 of the amount of protein normally present in an ejaculate [17]. Results of recent studies document that OIF in seminal plasma is a protein molecule with a molecular mass of 14 kDa that is resistant to heat and enzymatic digestion with proteinase K [18], [19].

The objective of the present study was to determine the effects of purified OIF on ovarian function in cattle, as a representative species of spontaneous ovulators. We tested the hypothesis that OIF will induce ovulation and affect CL form and function in cattle (Experiment 1). Based on the results of Experiment 1, we subsequently tested the hypothesis that OIF, given at various stages of development of the first follicular wave, will induce atresia of the dominant follicle and hasten emergence of a new follicular wave (Experiment 2).

Section snippets

Materials and methods

All animal experiment protocols were reviewed and approved by the University of Saskatchewan animal care committee.

Experiment 1—effect of OIF in prepubertal heifers

No effect of replicate was detected for any endpoint; therefore, data from Replicates 1 and 2 were combined. The diameter of the dominant follicle at the time of treatment did not differ among groups, but the proportion of heifers that ovulated in response to treatment (i.e., within 3 d of treatment) was greater (P < 0.05) in the GnRH-treated group than in the OIF- and saline-treated groups (Table 1). The interval from treatment to wave emergence was earlier in GnRH- and OIF-treated heifers

Discussion

Two experiments were conducted to determine the effect of OIF in cattle. Prepubertal heifers were used as a first approach, to avoid the confounding effects of spontaneous ovulation and elevated circulating concentrations of progesterone, and as an attempt to imitate the physiological conditions of the unmated llama—an induced ovulator. Although no ovulations were detected, OIF treatment was associated with suppression of the existing dominant follicle, a subsequent rise in circulating FSH

Acknowledgments

The project was supported by grants from the Natural Sciences and Engineering Research Council of Canada, the Alpaca Research Foundation and donations from members of the Canadian Llama and Alpaca Association.

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