Pheromonal bile acid 3-ketopetromyzonol sulfate primes the neuroendocrine system in sea lamprey

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.

Effects of Sex Pheromones and Sexual Maturation on Locomotor Activity in Female Sea Lamprey (Petromyzon marinus)

“…3kPZS has also been shown to have effects on differential systems in male and female sea lamprey. In male sea lamprey, it has been shown that 3kPZS has a greater effect on the endocrine system (Chung-Davidson et al, 2013; Siefkes et al, 2005), whereas in females it has a greater effect on the locomotor system (Li et al, 2002; Johnson et al, 2009). In our study, the measured change between the treatment and control was the presence of 3kPZS.…”

Chemical cues and pheromones in the sea lamprey (Petromyzon marinus)

“…Migratory sea lamprey are acutely tuned to the larval odor ( migratory cue ); putative components are detected at low concentrations [ 50 ] and larval odor elicits behavioral responses at the concentrations produced by a single larvae diluted several thousand fold [ 51 ]. Once sea lamprey arrive at the spawning grounds, final sexual maturation is partially triggered by conspecific odors [ 52 , 53 ]. Upon complete sexual maturation, mate search and spawning are guided by the odors of the opposite sex [ 11 ].…”

“…The male mating pheromone mediates pre-spawning upstream migration [ 88 ] and sexual maturation in males and females [ 52 ], and spawning upstream movement [ 54 ] and a suite of spawning behaviors in females [ 56 ]. The response elicited depends upon the spatial, environmental, and physiological context.…”

“…Pre-spawning upstream migration of males and females is reduced at low temperatures [ 89 , 90 ], but maintained in the presence of 3kPZS [ 88 ]. Mature male odor facilitates sexual maturation of males and females [ 52 ]. Sexually mature females display strong odor-conditioned rheotaxis in response to male odor, primarily in response to 3kPZS [ 54 – 56 ].…”

Integrative Neuro-Endocrine Pathways in the Control of Reproduction in Lamprey: A Brief Review

“…Recent evidence suggests that chemosensory input induce upregulation of GnRH expression in the lamprey brain followed by the downstream activation of HPG pathway and increase in plasma steroid level (73). The pathways that connect olfactory input to activation of GnRH secretion in the preoptic area are not known.…”