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Open Access Highly Accessed Research article

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

Yu-Wen Chung-Davidson1, Huiyong Wang1, Michael J Siefkes12, Mara B Bryan13, Hong Wu14, Nicholas S Johnson15 and Weiming Li1*

Author Affiliations

1 Department of Fisheries and Wildlife, Michigan State University, 13 Natural Resources Building, 480 Wilson Road, East Lansing, MI, 48824, USA

2 Present address: Great Lakes Fishery Commission, 2100 Commonwealth Blvd., Suite 100, Ann Arbor, MI, 48105, USA

3 Present address: Energy Biosciences Institute, University of California, 130 Calvin Laboratory, MC 5230, Berkeley, CA, 94720, USA

4 Present address: Department of Microbiology & Immunology, School of Medicine, Emory University, Rollins Research Center G214, 201 Dowman Drive, Atlanta, Georgia, 30322, USA

5 Present address: USGS, Great Lakes Science Center, Hammond Bay Biological Station, 11188 Ray Road, Millersburg, MI, 49759, USA

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BMC Neuroscience 2013, 14:11  doi:10.1186/1471-2202-14-11

Published: 20 January 2013

Abstract

Background

Vertebrate 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.

Results

The 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.

Conclusions

We conclude that a single male pheromone component primes the HPG axis in immature sea lamprey in a sexually dimorphic manner.

Keywords:
Pheromone; Priming; HPG axis; GnRH; Steroid; Sexual dimorphism