A mechanistic model for studying the initiation of anguillid vitellogenesis by comparing the European eel (Anguilla anguilla) and the shortfinned eel (A. australis)

P. Jéhannet, L. Kruijt, E.L. Damsteegt, W. Swinkels, L.T.N. Heinsbroek, P.M. Lokman, A.P. Palstra

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

An inverse relation exists between the maturation stage at the start of the oceanic reproductive migration and the migration distance to the spawning grounds for the various eel species. The European eel Anguilla anguilla migrates up to 5–6000 km and leaves in a previtellogenic state. The shortfinned eel A. australis migrates 2–4000 km and leaves in an early vitellogenic state. In this study, we compared the early pubertal events in European silver eels with those in silver shortfinned eels to gain insights into the initiation of vitellogenesis. Immediately after being caught, yellow and silver eels of both species were measured and sampled for blood and tissues. Eye index (EI), gonadosomatic index (GSI) and hepatosomatic index (HSI) were calculated. Plasma 11-ketotestosterone (11-KT) and 17β-estradiol (E2) levels were measured by radioimmunoassay. Pituitary, liver and ovaries were dissected for quantitative real-time PCR analyses (pituitary dopamine 2b receptor d2br, gonadotropin-releasing hormone receptors 1 and 2 gnrhr1 and gnrhr2, growth hormone gh and follicle-stimulating hormone-β fshb; liver estrogen receptor 1 esr1; gonad follicle-stimulating hormone receptor fshr, androgen receptors α and β ara and arb, vitellogenin receptor vtgr and P450 aromatase cyp19). Silver eels of both species showed a drop in pituitary gh expression, progressing gonadal development (GSI of ∼1.5 in European eels and ∼3.0 in shortfinned eels) and steroid level increases. In shortfinned eels, but not European eels, expression of fshb, gnrhr1 and gnrhr2, and d2br in the pituitary was up-regulated in the silver-stage as compared to yellow-stage females, as was expression of fshr, ara and arb in the ovaries. Expression of esr1 in European eels remained low while esr1 expression was up-regulated over 100-fold in silver shortfinned eels. The mechanistic model for anguillid vitellogenesis that we present suggests a first step that involves a drop in Gh and a second step that involves Fsh increase when switching in the life history trade-off from growth to reproduction. The drop in Gh is associated with gonadal development and plasma steroid increase but precedes brain-pituitary-gonad axis (BPG) activation. The Fsh increase marks BPG activation and increased sensitivity of the liver to estrogenic stimulation, but also an increase in D2br-mediated dopaminergic signaling to the pituitary.

LanguageEnglish
Pages129-138
JournalGeneral and Comparative Endocrinology
Volume279
DOIs
Publication statusPublished - 20 Feb 2019

Fingerprint

Anguilla
Vitellogenesis
Eels
Anguilla anguilla
mechanistic models
vitellogenesis
eel
Silver
silver
gonads
gonadosomatic index
Gonads
liver
steroids
brain
receptors
hepatosomatic index
Anguilla australis
follicle-stimulating hormone
vitellogenin

Keywords

  • Brain-pituitary-gonad axis
  • Dopaminergic inhibition
  • Eel reproduction
  • Growth hormone
  • Sex steroids
  • Silvering

Cite this

@article{c75a9045dd5a411a98c95f92f23fbfea,
title = "A mechanistic model for studying the initiation of anguillid vitellogenesis by comparing the European eel (Anguilla anguilla) and the shortfinned eel (A. australis)",
abstract = "An inverse relation exists between the maturation stage at the start of the oceanic reproductive migration and the migration distance to the spawning grounds for the various eel species. The European eel Anguilla anguilla migrates up to 5–6000 km and leaves in a previtellogenic state. The shortfinned eel A. australis migrates 2–4000 km and leaves in an early vitellogenic state. In this study, we compared the early pubertal events in European silver eels with those in silver shortfinned eels to gain insights into the initiation of vitellogenesis. Immediately after being caught, yellow and silver eels of both species were measured and sampled for blood and tissues. Eye index (EI), gonadosomatic index (GSI) and hepatosomatic index (HSI) were calculated. Plasma 11-ketotestosterone (11-KT) and 17β-estradiol (E2) levels were measured by radioimmunoassay. Pituitary, liver and ovaries were dissected for quantitative real-time PCR analyses (pituitary dopamine 2b receptor d2br, gonadotropin-releasing hormone receptors 1 and 2 gnrhr1 and gnrhr2, growth hormone gh and follicle-stimulating hormone-β fshb; liver estrogen receptor 1 esr1; gonad follicle-stimulating hormone receptor fshr, androgen receptors α and β ara and arb, vitellogenin receptor vtgr and P450 aromatase cyp19). Silver eels of both species showed a drop in pituitary gh expression, progressing gonadal development (GSI of ∼1.5 in European eels and ∼3.0 in shortfinned eels) and steroid level increases. In shortfinned eels, but not European eels, expression of fshb, gnrhr1 and gnrhr2, and d2br in the pituitary was up-regulated in the silver-stage as compared to yellow-stage females, as was expression of fshr, ara and arb in the ovaries. Expression of esr1 in European eels remained low while esr1 expression was up-regulated over 100-fold in silver shortfinned eels. The mechanistic model for anguillid vitellogenesis that we present suggests a first step that involves a drop in Gh and a second step that involves Fsh increase when switching in the life history trade-off from growth to reproduction. The drop in Gh is associated with gonadal development and plasma steroid increase but precedes brain-pituitary-gonad axis (BPG) activation. The Fsh increase marks BPG activation and increased sensitivity of the liver to estrogenic stimulation, but also an increase in D2br-mediated dopaminergic signaling to the pituitary.",
keywords = "Brain-pituitary-gonad axis, Dopaminergic inhibition, Eel reproduction, Growth hormone, Sex steroids, Silvering",
author = "P. J{\'e}hannet and L. Kruijt and E.L. Damsteegt and W. Swinkels and L.T.N. Heinsbroek and P.M. Lokman and A.P. Palstra",
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language = "English",
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A mechanistic model for studying the initiation of anguillid vitellogenesis by comparing the European eel (Anguilla anguilla) and the shortfinned eel (A. australis). / Jéhannet, P.; Kruijt, L.; Damsteegt, E.L.; Swinkels, W.; Heinsbroek, L.T.N.; Lokman, P.M.; Palstra, A.P.

In: General and Comparative Endocrinology, Vol. 279, 20.02.2019, p. 129-138.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - A mechanistic model for studying the initiation of anguillid vitellogenesis by comparing the European eel (Anguilla anguilla) and the shortfinned eel (A. australis)

AU - Jéhannet, P.

AU - Kruijt, L.

AU - Damsteegt, E.L.

AU - Swinkels, W.

AU - Heinsbroek, L.T.N.

AU - Lokman, P.M.

AU - Palstra, A.P.

PY - 2019/2/20

Y1 - 2019/2/20

N2 - An inverse relation exists between the maturation stage at the start of the oceanic reproductive migration and the migration distance to the spawning grounds for the various eel species. The European eel Anguilla anguilla migrates up to 5–6000 km and leaves in a previtellogenic state. The shortfinned eel A. australis migrates 2–4000 km and leaves in an early vitellogenic state. In this study, we compared the early pubertal events in European silver eels with those in silver shortfinned eels to gain insights into the initiation of vitellogenesis. Immediately after being caught, yellow and silver eels of both species were measured and sampled for blood and tissues. Eye index (EI), gonadosomatic index (GSI) and hepatosomatic index (HSI) were calculated. Plasma 11-ketotestosterone (11-KT) and 17β-estradiol (E2) levels were measured by radioimmunoassay. Pituitary, liver and ovaries were dissected for quantitative real-time PCR analyses (pituitary dopamine 2b receptor d2br, gonadotropin-releasing hormone receptors 1 and 2 gnrhr1 and gnrhr2, growth hormone gh and follicle-stimulating hormone-β fshb; liver estrogen receptor 1 esr1; gonad follicle-stimulating hormone receptor fshr, androgen receptors α and β ara and arb, vitellogenin receptor vtgr and P450 aromatase cyp19). Silver eels of both species showed a drop in pituitary gh expression, progressing gonadal development (GSI of ∼1.5 in European eels and ∼3.0 in shortfinned eels) and steroid level increases. In shortfinned eels, but not European eels, expression of fshb, gnrhr1 and gnrhr2, and d2br in the pituitary was up-regulated in the silver-stage as compared to yellow-stage females, as was expression of fshr, ara and arb in the ovaries. Expression of esr1 in European eels remained low while esr1 expression was up-regulated over 100-fold in silver shortfinned eels. The mechanistic model for anguillid vitellogenesis that we present suggests a first step that involves a drop in Gh and a second step that involves Fsh increase when switching in the life history trade-off from growth to reproduction. The drop in Gh is associated with gonadal development and plasma steroid increase but precedes brain-pituitary-gonad axis (BPG) activation. The Fsh increase marks BPG activation and increased sensitivity of the liver to estrogenic stimulation, but also an increase in D2br-mediated dopaminergic signaling to the pituitary.

AB - An inverse relation exists between the maturation stage at the start of the oceanic reproductive migration and the migration distance to the spawning grounds for the various eel species. The European eel Anguilla anguilla migrates up to 5–6000 km and leaves in a previtellogenic state. The shortfinned eel A. australis migrates 2–4000 km and leaves in an early vitellogenic state. In this study, we compared the early pubertal events in European silver eels with those in silver shortfinned eels to gain insights into the initiation of vitellogenesis. Immediately after being caught, yellow and silver eels of both species were measured and sampled for blood and tissues. Eye index (EI), gonadosomatic index (GSI) and hepatosomatic index (HSI) were calculated. Plasma 11-ketotestosterone (11-KT) and 17β-estradiol (E2) levels were measured by radioimmunoassay. Pituitary, liver and ovaries were dissected for quantitative real-time PCR analyses (pituitary dopamine 2b receptor d2br, gonadotropin-releasing hormone receptors 1 and 2 gnrhr1 and gnrhr2, growth hormone gh and follicle-stimulating hormone-β fshb; liver estrogen receptor 1 esr1; gonad follicle-stimulating hormone receptor fshr, androgen receptors α and β ara and arb, vitellogenin receptor vtgr and P450 aromatase cyp19). Silver eels of both species showed a drop in pituitary gh expression, progressing gonadal development (GSI of ∼1.5 in European eels and ∼3.0 in shortfinned eels) and steroid level increases. In shortfinned eels, but not European eels, expression of fshb, gnrhr1 and gnrhr2, and d2br in the pituitary was up-regulated in the silver-stage as compared to yellow-stage females, as was expression of fshr, ara and arb in the ovaries. Expression of esr1 in European eels remained low while esr1 expression was up-regulated over 100-fold in silver shortfinned eels. The mechanistic model for anguillid vitellogenesis that we present suggests a first step that involves a drop in Gh and a second step that involves Fsh increase when switching in the life history trade-off from growth to reproduction. The drop in Gh is associated with gonadal development and plasma steroid increase but precedes brain-pituitary-gonad axis (BPG) activation. The Fsh increase marks BPG activation and increased sensitivity of the liver to estrogenic stimulation, but also an increase in D2br-mediated dopaminergic signaling to the pituitary.

KW - Brain-pituitary-gonad axis

KW - Dopaminergic inhibition

KW - Eel reproduction

KW - Growth hormone

KW - Sex steroids

KW - Silvering

U2 - 10.1016/j.ygcen.2019.02.018

DO - 10.1016/j.ygcen.2019.02.018

M3 - Article

VL - 279

SP - 129

EP - 138

JO - General and Comparative Endocrinology

T2 - General and Comparative Endocrinology

JF - General and Comparative Endocrinology

SN - 0016-6480

ER -