Elsevier

Theriogenology

Volume 77, Issue 9, June 2012, Pages 1873-1882
Theriogenology

Research article
Ovarian estradiol modulates the stimulatory effect of ovulation-inducing factor (OIF) on pituitary LH secretion in llamas

https://doi.org/10.1016/j.theriogenology.2012.01.004Get rights and content

Abstract

This study was designed to: 1) characterize the effect of ovulation-inducing factor (OIF) on pituitary LH secretion in ovariectomized (OVX) llamas; and 2) determine the effect of OIF on LH secretion in OVX llamas pretreated with estradiol-17β (E-17β) or estradiol benzoate (EB). In Experiment 1, intact and OVX llamas (n = 5 or 6 per group) were assigned to a two by two factorial design: 1) Intact llamas treated with 1 mL of phosphate buffered saline (PBS); 2) Intact llamas treated with 1 mg of purified OIF; 3) OVX llamas treated with 1 mL of PBS; or 4) OVX llamas treated with 1 mg of purified OIF. In Experiment 2, intact and OVX llamas (n = 5 or 6 per group) were randomly assigned to the following groups: 1) Intact llamas treated with 1 mg of purified OIF; 2) OVX llamas treated with 1.0 mL of PBS; 3) OVX llamas treated with 1.0 mg of purified OIF; 4) OVX llamas primed with E-17β, followed by 1.0 mg of purified OIF. Experiment 3 was similar as described for Experiment 2, except that priming was done with EB. In Experiment 1, animal category by treatment and animal category by treatment by time interactions tended (P = 0.08) to affect LH concentration. The effect of OIF on LH released was partly restored (P < 0.05), to the values observed for the intact OIF-treated females, when OVX llamas were primed with E-17β or BE (Experiments 2 and 3). We concluded that peripheral estradiol concentrations in llamas partially modulates the effect of OIF on pituitary LH secretion; however, other ovarian factor(s) could also participate in this modulatory action.

Introduction

South American camelids have been classified as induced-ovulating species, based on early classical studies where penile intromission was considered the only stimuli responsible to induce ovulation in llamas and alpacas [1], [2]. However, the mechanism of ovulation in camelids has been challenged in recent studies, since the effect of a factor present in the seminal plasma has been proven to play an important role in the ovulation mechanism in these species. In contrast to other induced ovulators, such as rabbits, the vigorous mechanical stimulation of the vagina, cervix and uterus in alpacas, using a catheter, did not elicit ovulation in any of the stimulated females [3], supporting the notion that other copula-related stimulus, different and independent from physical, are responsible of induced ovulation in these species.

Several studies in llamas and alpacas [3], [4], [5], [6], [7], [8] documented that a protein factor present in the seminal plasma consistently induces an LH surge and consequently ovulation, when given by intramuscular or intravaginal deposition, in the absence of any genital physical stimulation. The biological active fraction of llama seminal plasma was identified as a robust protein, resistant to heat treatment and enzymatic digestion, and was denominated ovulation-inducing factor (OIF) [5]. Further purification procedures have identified a 14-kDa protein molecule from the seminal plasma of llamas [6].

Intramuscular administration of homologous whole seminal plasma in llamas [4], [7], [8] and alpacas [3], [7] induces ovulation in a high proportion (≥90%) of females. The same effect is observed after intramuscular administration of a seminal bioactive protein faction [5] and a purified isolated seminal protein molecule [6], [9]. Increased systemic LH concentrations, similar to those after natural mating [10], were documented after seminal plasma or purified OIF treatment [6], [7], [9], [11]. Moreover, a dose–response effect of llama OIF on pituitary LH release and ovulatory response was reported [9], demonstrating that the minimum amount of OIF required to induce ovulation was physiologically relevant in terms of the amount present in an ejaculate.

In a recent llama study [11], the effect of OIF on LH release was completely suppressed in females previously treated with a GnRH antagonist (cetrorelix), suggesting that OIF could act, in a direct or indirect fashion, on the GnRH hypothalamic neurons to trigger pituitary LH release. Ovarian steroids exert a modulatory effect on the mediobasal hypothalamic neurons network, to influence GnRH pulse secretion, in spontaneous ovulators [12], [13]. A similar effect has been suggested in several induced ovulating-species [14], [15].

Plasma estradiol concentrations correlate positively with follicular growth in llamas and alpacas, reaching maximum values just before the plateau of follicle growth [16], [17], [18], [19]. It has been suggested that the magnitude of preovulatory LH surge induced by mating in llamas and alpacas is dependent on follicular size and correlated to plasma estradiol concentration [16]. Therefore, we hypothesized that although the rise of peripheral estradiol concentration does not trigger ovulation in these species, it could however modulate the OIF-induced pituitary LH release.

The present study was designed to: 1) characterize the effect of OIF on pituitary LH secretion in ovariectomized (OVX) llamas; and 2) determine the effect of OIF on LH secretion in OVX llamas pretreated with estradiol-17β (E-17β) or estradiol benzoate (EB).

Section snippets

Materials and methods

The present study was conducted during April to July 2010 at the Universidad Austral de Chile, Valdivia, Chile (39°38′ S - 73°5′ W and 19 m above sea level). All procedures were reviewed and approved by the Universidad Austral de Chile Bioethics Committee and were performed in accordance with the animal care protocols established by the Universidad Austral de Chile.

Results

Because of complications in catheter placement, one llama from the OVX-OIF and OVX-E17β-OIF group, respectively were removed from Experiment 2 after 30 min of blood sampling for LH measurement and their data were excluded from further analysis.

Discussion

The effect of OIF on LH release was affected after intramuscular administration in ovariectomized llamas, highlighting the role of the ovary on the modulation of the hypothalamus or pituitary response to OIF. Additionally, the administration of exogenous estradiol to ovariectomized llamas is able to partially restore the magnitude of pituitary LH secretion when comparing to that observed in intact females, suggesting that plasma estradiol concentration affects pituitary LH secretion triggered

Acknowledgments

This study was supported by the Chilean National Science and Technology Research Council (Fondecyt 11080141). M. Silva is a Ph.D. student supported by a scholarship from Conicyt (Government of Chile) at the Faculty of Veterinary Sciences, Universidad Austral de Chile. We thank Marcos G. Colazo from Alberta Agriculture and Rural Development, Edmonton, AB, Canada for his collaboration in the statistical analyses.

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