Dopaminergic systems in the European eel: characterization, brain distribution, and potential role in migration and reproduction

Sébert, Marie-Emilie; Weltzien, Finn‐Arne; Moisan, C.; Pasqualini, Catherine; Dufour, Sylvie

doi:10.1007/978-1-4020-8548-2_3

Cited by 4 publications

(5 citation statements)

References 129 publications

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“…According to the morphology and location, double labeled CldU-TH newborn cells of the OB of G. omarorum correspond to granule cells of the ICL as shown in other teleosts ( Dicentrarchus labrax : Batten et al, 1993 ; D. rerio : Byrd and Brunjes, 1995 ; and Solea senegalensis : Rodríguez-Gómez et al, 2000 ). However, this is not coincident with the distribution of catecholaminergic neurons in the OB of A. leptorhynchus (Sas et al, 1990 ), D. rerio (Adolf et al, 2006 ), and D. labrax (Sébert et al, 2008 ) as in these species TH positive cells are almost absent in the ICL and more abundant in outer layers.…”

Section: Discussionmentioning

confidence: 94%

Cell Proliferation, Migration, and Neurogenesis in the Adult Brain of the Pulse Type Weakly Electric Fish, Gymnotus omarorum

2017

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Adult neurogenesis, an essential mechanism of brain plasticity, enables brain development along postnatal life, constant addition of new neurons, neuronal turnover, and/or regeneration. It is amply distributed but negatively modulated during development and along evolution. Widespread cell proliferation, high neurogenic, and regenerative capacities are considered characteristics of teleost brains during adulthood. These anamniotes are promising models to depict factors that modulate cell proliferation, migration, and neurogenesis, and might be intervened to promote brain plasticity in mammals. Nevertheless, the migration path of derived cells to their final destination was not studied in various teleosts, including most weakly electric fish. In this group adult brain morphology is attributed to sensory specialization, involving the concerted evolution of peripheral electroreceptors and electric organs, encompassed by the evolution of neural networks involved in electrosensory information processing. In wave type gymnotids adult brain morphology is proposed to result from lifelong region specific cell proliferation and neurogenesis. Consistently, pulse type weakly electric gymnotids and mormyrids show widespread distribution of proliferation zones that persists in adulthood, but their neurogenic potential is still unknown. Here we studied the migration process and differentiation of newborn cells into the neuronal phenotype in the pulse type gymnotid Gymnotus omarorum. Pulse labeling of S-phase cells with 5-Chloro-2′-deoxyuridine thymidine followed by 1 to 180 day survivals evidenced long distance migration of newborn cells from the rostralmost telencephalic ventricle to the olfactory bulb, and between layers of all cerebellar divisions. Shorter migration appeared in the tectum opticum and torus semicircularis. In many brain regions, derived cells expressed early neuronal markers doublecortin (chase: 1–30 days) and HuC/HuD (chase: 7–180 days). Some newborn cells expressed the mature neuronal marker tyrosine hydroxylase in the subpallium (chase: 90 days) and olfactory bulb (chase: 180 days), indicating the acquisition of a mature neuronal phenotype. Long term CldU labeled newborn cells of the granular layer of the corpus cerebelli were also retrogradely labeled “in vivo,” suggesting their insertion into the neural networks. These findings evidence the neurogenic capacity of telencephalic, mesencephalic, and rhombencephalic brain proliferation zones in G. omarorum, supporting the phylogenetic conserved feature of adult neurogenesis and its functional significance.

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Section: Discussionmentioning

confidence: 94%

Cell Proliferation, Migration, and Neurogenesis in the Adult Brain of the Pulse Type Weakly Electric Fish, Gymnotus omarorum

2017

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“…As reviewed by Sébert et al. (63), measuring TH protein/enzymatic activity and DA and metabolite levels would give further information on melatonin treatment effects on TH and DA activity in the eel. In mammals, most of the studies have focused on melatonin effects on the dopaminergic nigrostriatal system aiming to investigate its potential neuroprotective property in neurodegenerative diseases such as Parkinson’s disease (64).…”

Section: Discussionmentioning

confidence: 99%

Melatonin Activates Brain Dopaminergic Systems in the Eel with an Inhibitory Impact on Reproductive Function

Sébert

Legros

Weltzien

et al. 2008

J Neuroendocrinology

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In the eel, a deficit in gonadotrophin-releasing hormone (GnRH) and a strong dopaminergic (DA) inhibition are responsible for the blockade of gonad development if silver eels are prevented from their reproductive migration. Environmental factors that eels encounter during their oceanic reproductive migration are thought to play an important role in the stimulation of eel pubertal development. We investigated the potential role of melatonin, a known mediator of the effects of external factors on reproductive function in vertebrates. We demonstrated that a long-term melatonin treatment increased brain tyrosine hydroxylase (TH, the rate limiting enzyme of DA synthesis) mRNA expression in a region-dependent way. Melatonin stimulated the dopaminergic system of the preoptic area, which is involved in the inhibitory control of gonadotrophin [luteinising hormone (LH) and follicle-stimulating hormone (FSH)] synthesis and release. Moreover, we showed that the increased TH expression appeared to be consistent with melatonin binding site distribution as shown by 2[(125)I]-melatonin labelling studies. On the other hand, melatonin had no effects on the two eel native forms of GnRH (mGnRH and cGnRH-II) mRNA expression. Concerning the pituitary-gonad axis, we showed that melatonin treatment decreased both gonadotrophin beta-subunit (LHbeta, FSHbeta) mRNA expression and reduced sexual steroid (11-ketotestosterone, oestradiol) plasma levels. This indicates that melatonin treatment had a negative effect on eel reproductive function. To our knowledge, the results of the present study provide the first evidence that melatonin enhances TH expression in specific brain regions in a non-mammalian species. By this mechanism melatonin could represent one pathway by which environmental factors could modulate reproductive function in the eel.

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“…Indeed, when A. anguilla received sustained treatments with GnRH agonist, DA‐D2 receptor antagonist (pimozide) and steroids [testosterone (T) or E 2 ], alone or in combination, only the triple treatment with steroid, GnRH agonist and pimozide could induce dramatic increases in LH synthesis and release, as well as in vitellogenin (Vg) plasma levels and a stimulation of ovarian vitellogenesis (Dufour et al , 1988; Vidal et al , 2004). Immunocytochemistry, in situ hybridization and retrograde tracing were used to map DA neurones and projections in the brain and pituitary (Sébert et al , 2008 a ). These studies showed that in A. anguilla DA neurones originating from the NPOav project to the pars distalis of the pituitary where gonadotrophs are located (Vidal et al , 2004; Sébert et al , 2008 a ) (Fig.…”

Section: Inhibitory Role Of Dopamine In the Neuroendocrine Control Ofmentioning

confidence: 99%

“…Immunocytochemistry, in situ hybridization and retrograde tracing were used to map DA neurones and projections in the brain and pituitary (Sébert et al , 2008 a ). These studies showed that in A. anguilla DA neurones originating from the NPOav project to the pars distalis of the pituitary where gonadotrophs are located (Vidal et al , 2004; Sébert et al , 2008 a ) (Fig. 1).…”

Section: Inhibitory Role Of Dopamine In the Neuroendocrine Control Ofmentioning

confidence: 99%

“…Dopaminergic activity can be regulated at different levels either by regulating DA biosynthesis, DA metabolism (degradation, reuptake) or DA binding to its target cells. DA biosynthesis and turnover may be assessed using various methods among which evaluation of metabolites to neurotransmitter ratios (Sébert et al , 2008 a ). In fishes, however, the levels of DA metabolites and their relative importance in the assessment of DA catabolism maybe controversial (Hernandez‐Rauda et al , 1996).…”

Section: Regulation Of Dopaminergic Inhibitionmentioning

confidence: 99%

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Neuroendocrine control by dopamine of teleost reproduction

Dufour

Sébert

Weltzien

et al. 2010

Journal of Fish Biology

141

123

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While gonadotropin-releasing hormone (GnRH) is considered as the major hypothalamic factor controlling pituitary gonadotrophins in mammals and most other vertebrates, its stimulatory actions may be opposed by the potent inhibitory actions of dopamine (DA) in teleosts. This dual neuroendocrine control of reproduction by GnRH and DA has been demonstrated in various, but not all, adult teleosts, where DA participates in an inhibitory role in the neuroendocrine regulation of the last steps of gametogenesis (final oocyte maturation and ovulation in females and spermiation in males). This has major implications for inducing spawning in aquaculture. In addition, DA may also play an inhibitory role during the early steps of gametogenesis in some teleost species, and thus interact with GnRH in the control of puberty. Various neuroanatomical investigations have shown that DA neurones responsible for the inhibitory control of reproduction originate in a specific nucleus of the preoptic area (NPOav) and project directly to the region of the pituitary where gonadotrophic cells are located. Pharmacological studies showed that the inhibitory effects of DA on pituitary gonadotrophin production are mediated by DA-D2 type receptors. DA-D2 receptors have now been sequenced in several teleosts, and the coexistence of several DA-D2 subtypes has been demonstrated in a few species. Hypophysiotropic DA activity varies with development and reproductive cycle and probably is controlled by environmental cues as well as endogenous signals. Sex steroids have been shown to regulate dopaminergic systems in several teleost species, affecting both DA synthesis and DA-D2 receptor expression. This demonstrates that sex steroid feedbacks target DA hypophysiotropic system, as well as the other components of the brain-pituitary gonadotrophic axis, GnRH and gonadotrophins. Recent studies have revealed that melatonin modulates the activity of DA systems in some teleosts, making the melatonin-DA pathway a prominent relay between environmental cues and control of reproduction. The recruitment of DA neurons for the neuroendocrine control of reproduction provides an additional brain pathway for the integration of various internal and environmental cues. The plasticity of the DA neuroendocrine role observed in teleosts may have contributed to their large diversity of reproductive cycles.

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Dopaminergic systems in the European eel: characterization, brain distribution, and potential role in migration and reproduction

Cited by 4 publications

References 129 publications

Cell Proliferation, Migration, and Neurogenesis in the Adult Brain of the Pulse Type Weakly Electric Fish, Gymnotus omarorum

Cell Proliferation, Migration, and Neurogenesis in the Adult Brain of the Pulse Type Weakly Electric Fish, Gymnotus omarorum

Melatonin Activates Brain Dopaminergic Systems in the Eel with an Inhibitory Impact on Reproductive Function

Neuroendocrine control by dopamine of teleost reproduction

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