Abstract
BackgroundVertebrate pheromones are known to prime the endocrine system, especially the hypothalamic-pituitary-gonadal (HPG) axis. However, no known pheromone molecule has been shown to modulate directly the synthesis or release of gonadotropin releasing hormone (GnRH), the main regulator of the HPG axis. We selected sea lamprey (Petromyzon marinus) as a model system to determine whether a single pheromone component alters the output of GnRH.Sea lamprey male sex pheromones contain a main component, 7α, 12α, 24-trihydroxy-5α-cholan-3-one 24-sulfate (3 keto-petromyzonol sulfate or 3kPZS), which has been shown to modulate behaviors of mature females. Through a series of experiments, we tested the hypothesis that 3kPZS modulates both synthesis and release of GnRH, and subsequently, HPG output in immature sea lamprey.ResultsThe results showed that natural male pheromone mixtures induced differential steroid responses but facilitated sexual maturation in both sexes of immature animals (χ2 = 5.042, dF = 1, p < 0.05). Exposure to 3kPZS increased plasma 15α-hydroxyprogesterone (15α-P) concentrations (one-way ANOVA, p < 0.05) and brain gene expressions (genes examined: three lamprey (l) GnRH-I transcripts, lGnRH-III, Jun and Jun N-terminal kinase (JNK); one-way ANOVA, p < 0.05), but did not alter the number of GnRH neurons in the hypothalamus in immature animals. In addition, 3kPZS treatments increased lGnRH peptide concentrations in the forebrain and modulated their levels in plasma. Overall, 3kPZS modulation of HPG axis is more pronounced in immature males than in females.ConclusionsWe conclude that a single male pheromone component primes the HPG axis in immature sea lamprey in a sexually dimorphic manner.
Highlights
Vertebrate pheromones are known to prime the endocrine system, especially the hypothalamicpituitary-gonadal (HPG) axis
Immature females exposed to Spermiating male washing (SMW) began to ovulate in 21 days, whereas immature females exposed to prespermiating male washings (PSMW, no pheromone control) did not start to ovulate until day 40
Immature males showed an increase in 15α-P concentrations in response to SMW exposure early in the spawning season (May and June) while immature females did not show the decrease in response to SMW until mid-season (June) and the response dropped abruptly after July (Figure 1)
Summary
Exposure to 10-9 M 3kPZS only increased lGnRH-I transcript variants, lGnRH-III and Jun mRNA concentrations in the forebrain of immature males (Figure 3). Prolonged exposure to 10-10 M 3kPZS (48 h) increased GAP58 (1122-fold), lGnRH-III (826-fold), and JNK (2-fold) transcripts in the brain stem of immature males (Figure 4). Prolonged exposure to 10-9 M 3kPZS (48 h) decreased GAP49 (7-fold) but increased GAP58 (2735-fold) expressions in the brain stem of immature males (Figure 4). Differential effect of 3kPZS on forebrain and plasma lGnRH peptide concentrations Exposure to 10-10 M 3kPZS increased lGnRH-I and -III peptide concentrations in the forebrain (Figures 5 & 6) but had no effect in the brain stem of immature males (Additional file 1: Figures S1& S2). Exposure to 3kPZS had no effect on the number of lGnRH-I or -III immunoreactive cells in the preoptic-hypothalamic area
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