Abstract

The hypothalamic-pituitary system is considered to be a vertebrate innovation and seminal event that emerged prior to or during the differentiation of the ancestral agnathans. Lampreys are the earliest evolved vertebrates for which there is a demonstrated neuroendocrine system. Lampreys have three hypothalamic gonadotropin-releasing hormones (GnRHs; lGnRH-I, -II, and -III) and two and possibly three pituitary GnRH receptors involved in mediating reproductive processes. Estradiol is considered to be a major reproductive steroid in both male and female lampreys. The purpose of this study was to investigate estrogen receptor (ER) expression in the lamprey brain in adult sea lampreys. Expression of ER mRNA was confirmed in the adult lamprey brain using RT-PCR. Using digoxigenin (DIG)-labeled probes, ER expression was shown to yield moderate, but distinct reaction products in specific neuronal nuclei of the lamprey brain, including the olfactory lobe, hypothalamus, habenular area, and hindbrain. Expression of ER in the hypothalamic area of the brain provides evidence of potential interaction between estradiol and GnRH(s), and is consistent with previous evidence showing estrogen feedback on GnRH in adult lamprey brain. Earlier studies have reported that there is a close distribution of glutamic acid decarboxylase (GAD; GABA-synthesizing enzyme) and lamprey GnRH in the preoptic region in adult lampreys. The establishment of a direct estradiol–kisspeptin–GABA–GnRH interaction in lamprey has yet to be determined and will require future functional and co-localization studies. The phylogenetic position of lampreys as a basal vertebrate allows lampreys to be a basis for understanding the molecular evolution of the neuroendocrine system that arose in the vertebrates.

Highlights

  • Modern vertebrates are classified into two major groups, the gnathostomes and the agnathans

  • There is a general pattern of gonadotropin-releasing hormones (GnRHs) distribution in the anterior-preoptic-neurohypophysial tract to the neurohypophysis of adult lampreys as determined by several immunohistochemical (IHC) studies using specific GnRH antisera to each of the lamprey GnRHs and by in situ hybridization studies using specific GnRH probes (Crim et al, 1979a,b; Nozaki and Kobayashi, 1979; King et al, 1988; Nozaki et al, 1994; Reed et al, 2002; Kavanaugh et al, 2008)

  • In this study, estrogen receptor (ER) was shown to be expressed in the lamprey brain by RT-PCR and DIG-labeled in situ hybridization

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Summary

Introduction

Modern vertebrates are classified into two major groups, the gnathostomes (jawed vertebrates) and the agnathans (jawless vertebrates). It was shown that neurosecretory peptides like GnRH diffuse from the brain (neurohypophysis) to the adenohypophysis, and regulate its secretory activity in lampreys. There is evidence of normal occurrence of GnRH in a part of the lamprey brain homologous with that brain region in later evolved vertebrates in which GnRH localization forms part of a neuroendocrine mechanism for gonadotropin secretion. Neurosecretory peptides like GnRH are able to diffuse from the brain to the pituitary to regulate its secretory activity. Crim (1981) and King et al (1988) showed that GnRH neurons project into the third ventricle. These authors proposed an additional route of GnRH via secretion into the third www.frontiersin.org

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