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Biology of Reproduction 65, 1573-1578 (2001)
© 2001 Society for the Study of Reproduction, Inc.

Regular Article

Action of Leptin on In Vitro Luteinizing Hormone Release in the European Sea Bass (Dicentrarchus labrax)1

Pierre Peyona, Silvia Zanuya, and Manuel Carrillo2,a

a Department of Fish Reproductive Physiology, Instituto de Acuicultura de Torre de la Sal, Consejo Superior de Investigaciones Cientificas, 12595 Torre de la Sal, Castellon, Spain

ABSTRACT

The discovery of leptin has sparked a rapidly growing number of publications concerning the role of leptin in the regulation of body adiposity, feeding, and reproductive system in mammals. To date, there have been no reports on the presence of leptin-related peptide, and functional studies on the role of leptin remain limited in fishes. We investigated the effect of mouse recombinant leptin on basal and sea bream (sb) GnRH-induced LH release from dispersed pituitary cells obtained from male European sea bass (Dicentrarchus labrax) at different stages of sexual development. The potential interaction of leptin with the porcine neuropeptide Y (pNPY), known to play a dual role in feeding and reproduction in vertebrates, was also investigated. High doses of leptin (10–8–10-6 M) and/or pNPY (0.1 and 1 nM) had different effects on LH release at various stages of sexual development. Porcine NPY alone was weakly effective on basal LH release, but it enhanced LH release induced by leptin (10-6 M) in late prepuberty but not in early postpuberty. Additive or inhibitory effects of leptin were observed on sbGnRH-induced LH release depending on sbGnRH dose and stage of sexual development. The direct action of leptin on LH release at the pituitary level in sea bass suggests that leptin is a regulator of the reproductive system in fishes.

anterior pituitary, fish, gonadotropin-releasing hormone, leptin, luteinizing hormone, neuropeptide Y, puberty

INTRODUCTION

Identified in late 1994, leptin, a protein product of the obese (ob) gene secreted as a hormone from adipocytes, was first described as an "adipostat," a humoral signal carrying information regarding energy reserves, playing an important role in the regulation of body weight and metabolism in mammals [1–4]. More recent observations have suggested that leptin also plays an important role in neuroendocrine signalling and reproduction [5]. Concordant with its proposed role in relaying information about nutritional status, leptin fits many requirements for a molecule linking the regulation of energy balance and the control of reproduction [6]. In mammals, leptin receptors have been localized at the pituitary level, and leptin has been shown to increase gonadotropin secretion and plasma levels, both in vivo and in vitro [7, 8], independently of hypothalamic action. In vitro, GnRH release from the hypothalamus is stimulated by the presence of leptin in the medium [8]. The occurrence of leptin receptors in peripheral structures of the reproductive system suggests that, in addition to the hypothalamus and pituitary, leptin might also exert actions at these sites [9].

GnRH plays a central role in the neuroendocrine control of the reproductive process in vertebrates, including fishes, particularly by stimulating synthesis and release of gonadotropins. The existence of multiple molecular forms in the brain of teleosts has been well demonstrated [10, 11]. In sea bass, three different forms of GnRH are present: sea bream (sb) GnRH, chicken (c) GnRH-II, and salmon (s) GnRH [12]. However, sbGnRH, the most abundant form in the pituitary, seems to be the physiologically relevant isoform with respect to gonadotropin release in perciform fishes [13–18].

In addition to GnRH, pituitary LH is also stimulated by a number of neuroendocrine factors. In vertebrates, including fishes, the orexigenic peptide neuropeptide Y (NPY) is one of these factors and has been implicated in the hypothalamic regulation of reproduction and energy homeostasis. In addition to its hypothalamic action in modulating GnRH secretion in a sex steroid-dependent manner, NPY also acts directly on gonadotrophs of the anterior pituitary, thereby exerting a dual control on the regulation of LH secretion in mammals [19, 20]. In vitro and in vivo studies in fishes, have demonstrated that the NPY-induced LH response is dependent on reproductive status [21–28]. In European sea bass (Dicentrarchus labrax), in vivo and in vitro effects of NPY on LH secretion were recently demonstrated [29].

To date, leptin has only been characterized in endotherms, and the evolution of its function has been largely ignored. In the original report on the identification of the gene that encodes leptin [1], a genomic Southern blot hybridized with ob cDNA probe indicated the presence of a homologous DNA fragment in all vertebrates tested, including one teleost, the eel. More recently, Johnson et al. [30] suggested that a leptin gene homologue may be present in fishes. Nevertheless, functional studies on leptin are limited in fishes.

The European sea bass is a seasonal spawner and reaches sexual maturity at 2 (males) and 3 (females) yr of age [31]. The maximal food intake period of this species appears to be from late spring to early autumn. Food intake gradually declines during the period of gonadal development (October–December) to reach minimal values during the spawning period (December–March) [32]. This inverse pattern of annual distribution of ingestion and reproduction suggests that nutritional status may be involved in the modulation of the reproductive axis.

The aim of the present study was to investigate the potential action of leptin on puberty and adult reproductive function in sea bass. The effect of recombinant mouse leptin on basal and NPY- and sbGnRH-induced LH release was studied by using dispersed pituitary cell culture obtained from male sea bass at different stages of sexual development.

MATERIALS AND METHODS

Animals

Male European sea bass were obtained from Aquadrava (Tarragona, Spain; 2-yr-old fish) and GEDISA (Mallorca, Spain; 5-yr-old fish). Fish were maintained in 3000-L tank supplied with continuously aerated running seawater. Animals were acclimated for 1 mo under natural photoperiod and temperature conditions within the facilities of the Instituto de Acuicultura de Torre de la Sal (east coast of Spain, 40°N, 0°E) and were fed once daily to excess with a commercially prepared fish food (ProAqua, Palencia, Spain). The development stage of fish was based on the time of year and was confirmed by the gonadosomatic index (GSI). Young fish (2 yr old) were used at different reproductive stages: late prepubertal (December, body weight = 271 ± 17 g; GSI = 0.32 ± 0.11; n = 15), first spermiating (February, body weight = 306 ± 26 g; GSI = 1.03 ± 0.16; n = 15), and early postpubertal (March, body weight = 330 ± 11 g; GSI = 0.73 ± 0.21; n = 15). Adult fish (5 yr old) were at the prespermiating stage (December, body weight = 847 ± 55 g; GSI = 4.5 ± 0.3; n = 4).

Hormones and Chemicals

Unless otherwise indicated, all chemicals and compounds were purchased from Sigma (St. Louis, MO). Sea bream GnRH was kindly provided by Dr. Y. Zohar. Recombinant mouse leptin, porcine NPY (pNPY), and sbGnRH were prepared immediately before use.

Dispersed Pituitary Cell Culture

Fish were anesthetized using ice, and pituitaries (pool of 15 or four depending on the sexual development stage) were removed and placed in ice-cold dispersion medium (L-15 with Hanks salt, 25 mM Hepes, 0.5% BSA, 1% penicillin-streptomycin, and 0.1 mg/ml gentamicin, pH 7.4). Excised pituitaries were washed three times with dispersion medium (room temperature) and diced. Cells were enzymatically dispersed using a trypsin/DNase II digestion method modified from the method of Chang et al. [33]. Fragments were exposed in sequence to trypsin (type II, 25 mg/10 ml) for 40 min at room temperature with shaking, trypsin inhibitor (25 mg/10 ml, 10 min), and DNase II (0.1 mg/10 ml, 10 min). Following enzymatic treatment, fragments were mechanically dispersed by gentle suction and extrusion with a plastic transfer pipette in a dispersion medium. Dispersed cells were filtered through a nylon mesh (30-µm pore size) and harvested by centrifugation at 200 x g for 10 min. Harvested cells were then reconstitued in 5 ml of serum-free L-15, and the cell yield and viability were calculated by counting cells in a hemocytometer in the presence of trypan blue. The cell dispersion method yielded cells of 96%–98% viability. Because this cell dispersion method results in a mixed population of pituitary cells, immunocytochemistry using specific antibodies for sea bass ßLH subunit was performed to confirm that secretory gonadotrophs were present in the populations (data not shown).

Dispersed cells were cultured (2.5 x 105 cells well-1 ml-1) in primary 24-well culture plates (Falcon, Becton Dickinson, NJ) overnight at 20°C in culture medium (L-15 containing 10% fetal bovine serum, 0.1% BSA, 1% penicillin-streptomycin, and 0.1 mg/ml gentamincin, pH 7.4). The following day, medium was replaced with serum-free culture medium containing or not containing freshly diluted hormones (0.5 ml/well). Medium was removed 3 h after treatment and stored at -80°C until further analysis for LH content according to the method of Cerdá-Reverter et al. [29]. All treatments were performed in quadruplicate.

LH Measurements and Data Analysis

The LH levels in the culture medium were determined by an homologous ELISA [34] according to the method developed in striped bass by Mañanós et al. [35]. The sea bass LH ELISA included specific polyclonal antibodies against the sea bass LHß subunit and sea bass LH for the standard curve. The sensitivity of the assay was approximately 0.5 ng/ml, and the interassay coefficient of variation was approximately 15%. All data are expressed as mean values ± SEM and were compared by ANOVA followed by Student-Newman-Keuls multiple comparison tests. Differences wer considered significant at P < 0.05.

RESULTS

Effect of Leptin on LH Release

The time-course studies of recombinant mouse leptin effect on the LH release by pituitary cells obtained from male sea bass at first spermiating stage are shown in Figure 1. In control wells, LH release gradually rose as a function of incubation time from 31.87 ± 2.43 ng/ml to 63.45 ± 1.87 ng/ml after 1 h and 12 h of incubation, respectively. The addition of 10-10 M leptin did not alter basal LH levels. In the presence of 10-8 M leptin, the LH response exhibited a peak of release after 3 h of incubation, reaching 60.26 ± 5.30 ng/ml (P < 0.05 compared with controls). The presence of 10-6 M leptin induced a significant release of LH after 1 h of incubation (P < 0.05 compared with the other groups). This increase continued up to 3 h, becoming maximal at 241 ± 14 ng/ml. A decrement in the LH response induced by both 10-8 and 10-6 M leptin was then observed after 6 and 12 h of incubation, respectively.



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  		FIG. 1. Time course of in vitro LH responses to graded doses (10-10, 10-8, and 10-6 M) of recombinant mouse leptin in pituitary cells dispersed from sea bass at first spermiating stage. Results are expressed in ng/ml

The in vitro LH releases with graded doses of recombinant mouse leptin were examined in male sea bass at late prepubertal, early postpubertal, and adult (prespermiating) stages (Fig. 2). Data represent the LH release after 3 h of incubation expressed as a percentage of the basal release. Incubation of pituitary cells with leptin resulted in a dose-dependent stimulation of LH release at 3 h, and the magnitude of the response depended on the physiologic stage. In late prepubertal fish, 10-8 M leptin was significantly effective in inducing LH release of approximately 150%. The LH response to 10-6 M was greatly increased to approximately 520%. In early postpubertal and adult fish, LH response to leptin gradually increased with the dose of leptin but exhibited a significant increase at only 10-6 M leptin of approximately 160%–170%.



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  		FIG. 2. In vitro LH responses to graded doses of recombinant mouse leptin in pituitary cells dispersed from late prepubertal, early postpubertal, and adult sea bass after 3 h of incubation. Results are expressed as percentage increase over basal secretion. Basal levels for late prepubertal, early postpubertal, and adult fish were 14.74 ± 0.85 ng/ml, 8.98 ± 0.65 ng/ml, and 111.03 ± 13.07 ng/ml, respectively. Significant differences between groups are represented by different letters above the bars for each sampling point (P < 0.05)

Effect of pNPY and sbGnRH on LH Secretion

The presence of pNPY produced a significant increase of LH release in all reproductive stages tested (P < 0.05 compared with controls) (Fig. 3). A dose-dependent stimulation of LH release by pNPY was only observed in adult fish. The response to pNPY was similar in late prepubertal and early postpubertal fish; reaching approximately 130% of the basal release with the tested doses of pNPY. A dose-dependent effect of sbGnRH was observed, significantly effective from a dose of 0.1 nM, in all physiologic stages tested (Fig. 4). The magnitude of LH response varied according to the reproductive status of the fish. At 1 nM sbGnRH, LH release was increased by 1230%, 438%, and 543% in late prepubertal, early postpubertal, and adult fish, respectively.



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  		FIG. 3. Dose-response curves of pNPY effects associated or not with effects of recombinant mouse leptin (10-8 and 10-6 M) on in vitro LH release in dispersed pituitary cells obtained from late prepubertal, early postpubertal, and adult sea bass after 3 h of incubation. Results are expressed as percentage increase over basal release. Basal levels for late prepubertal, early postpubertal, and adult fish were 12.67 ± 0.73 ng/ml, 8.98 ± 0.65 ng/ml, and 111.03 ± 13.07 ng/ml, respectively



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  		FIG. 4. Dose-response curves of sbGnRH effects of recombinant mouse leptin (10-8 and 10-6 M) on in vitro LH release in dispersed pituitary cells obtained from late prepubertal, early postpubertal, and adult sea bass after 3 h of incubation. Results are expressed as percentage increase over basal release. Basal levels for late prepubertal, early postpubertal, and adult fish were 12.67 ± 0.73 ng/ml, 8.98 ± 0.65 ng/ml, and 111.03 ± 13.07 ng/ml, respectively

Leptin Effect on pNPY- and sbGnRH-Induced LH Secretion

The association of pNPY and 10-6 M leptin enhanced the LH response of pituitary cells obtained from late prepubertal fish compared with that obtained in the presence of each hormone alone (P < 0.05) (Fig. 3). No significant difference was observed in the presence of 10-8 M leptin at all stages. A synergistic effect was observed between pNPY and leptin in late prepubertal fish; LH response induced by the combination of 0.1 or 1 nM NPY and 10-6 M leptin was enhanced by approximately 1500%. In early postpubertal and adult fish, no synergistic effect was observed in the LH response obtained from the combination of pNPY and 10-6 M leptin.

No synergistic effect of leptin and sbGnRH on the LH response was observed regardless of the hormonal dose and the physiologic stage of fish (Fig. 4). An additive effect was exhibited by 10-6 M leptin on LH release induced by 0.1 nM of sbGnRH in the three stages. Furthermore, LH release induced by 1 nM of sbGnRH was either unaltered or inhibited in the presence of leptin.

DISCUSSION

The results of the present study demonstrate a direct action of leptin at the pituitary level on LH release in sea bass. In dispersed pituitary cell culture, leptin had a potent effect on LH release after 3 h of incubation, providing evidence of the ability of leptin to directly affect pituitary tissue. In addition, the magnitude of LH response differed depending on the stage of sexual development and was independent of the stimulation of sbGnRH, suggesting that there is a change in the sensitivity of gonadotrophs to leptin during sexual development of sea bass and that the mechanisms for stimulation of LH release by leptin and sbGnRH are different. Similarly, Weil et al. [36] previously described the long-term effect (2 days of incubation) of human leptin on gonadotropin in vitro secretion in trout. Consistent with our results, they also reported an effect dependent on the sexual status but independent of GnRH stimulation.

These results in fishes are consistent with data from mammals, reporting the stimulatory effect of leptin on gonadotropin release from rat pituitaries within 3 h of incubation [7]. However, as reported in trout [36], the leptin doses required to induce a significant LH response from sea bass pituitary cells were high compared with that (10-11 M) required in rat [7]. This apparent insensitivity of cells to leptin could be explained by the use of heterologous hormone. These findings provide additional evidence that leptin can play an important role, independent of the hypothalamic control of GnRH, in the neuroendocrine control of anterior pituitary function in fishes as well as in mammals.

It is well established that NPY affects the reproductive axis in a number of species, including rats [20]. This modulatory effect of NPY is potentially exerted at both the hypothalamus and the anterior pituitary [19], and the effect of NPY on LH secretion has been widely demonstrated in both mammals and fishes [20, 37]. Recently, Cerdá-Reverter et al. [29] reported a dose-dependent stimulation of pNPY on in vitro LH release in juvenile sea bass. In the present study, we found a stimulatory effect of pNPY on LH release of pituitary cells dispersed from late prepubertal and adult male fish, supporting the role of NPY in gonadotropin regulation at the pituitary level in sea bass.

It has been proposed that NPY mediates some of the effects of leptin in the control of feeding behavior and reproductive function. Leptin receptor is expressed by NPY neurons in the arcuate nucleus in mammals [38, 39]. In two studies, NPY and leptin showed permissive effects on the GnRH secretion in adult rat hypothalamus [40, 41]. Despite these investigations on the GnRH network, no studies have been conducted to examine a potential interaction between NPY and leptin in the control of secretion of LH at the pituitary level. The results of the present study are the first to show an interactive effect of NPY and leptin on the regulation of LH release in vertebrates. The effect of cotreatment with leptin and NPY was dependent on the course of natural reproductive development. Interestingly, a synergistic effect on LH response release was only observed in pituitary cells dispersed from late prepubertal fish. This fact can be linked to the high sensitivity of gonadotrophs to leptin in late prepubertal fish. We hypothesize that, as suggested in mammals, leptin/NPY differentially influence reproductive capability in two ways: 1) the timing of the onset of puberty and 2) the ability to maintain reproductive function during adulthood. Recent data indicate that leptin is capable of acting centrally to stimulate LH release but only during late juvenile development. Thus, leptin probably plays a facilitatory role in late juvenile LH secretion but does not drive the GnRH/LH releasing system to first ovulation and hence sexual maturity [42]. Although the physiologic relevance of this hypothesis remains to be determined, leptin effects probably reflect hormonal status changes (particularly in the sex steroid levels) during reproductive development.

In vertebrates, the LH-releasing activity of many neuropeptides and neurotransmitters is modulated by sex steroids that contribute to gonadal feedback and seasonal cyclicity of the various neuroendocrine systems. In the female rat, the central effects of leptin on gonadotropin release are strongly dependent on plasma estradiol levels [43]. Similarly, earlier data in mammals suggested that sex steroids modulate the effects of NPY on gonadotropin secretion from the anterior pituitary in addition to modulating NPY-induced GnRH release from the hypothalamus [20]. In fishes, the action of NPY on LH release varies with the seasonal reproductive cycle. In vitro and in vivo studies in female rainbow trout have demonstrated that the NPY-induced LH response is also dependent on reproductive status [21–23]. The action of NPY on LH release varies with the seasonal reproductive cycle in goldfish. NPY has a relatively low level of action on in vitro LH release from pituitaries in sexually regressed female goldfish compared with sexually mature fish, and the actions are enhanced in sexually regressed fish by implantation with estradiol and testosterone [44].

However, because the negative energetic periods in the sea bass are associated with the reproductive period, energetic modulation of NPY/leptin effects should be taken into account when considering the seasonality of induced LH secretion. In mammals, nutritional status influences reproductive function, and leptin-induced LH secretion is dependent on energetic status. Although intracerebroventricular leptin administration increased LH pulse amplitude in nonfasted rats [8], most in vivo studies have found an effect of leptin on gonadotropin secretion only in fasting animals [45, 46]. Although the effect of NPY on LH secretion has been widely demonstrated in mammals, no data on the effects of energetic status on NPY-modulated LH secretion are available. In sea bass, the NPY-induced LH secretion is dependent on energetic status [29]. Under negative energetic conditions imposed by chronic fasting, LH secretion in vivo was dose-dependently enhanced in response to pNPY. In contrast, positive energetic status suppressed the ability of NPY to increase plasma LH levels.

The present work provides functional evidence of the potential role of leptin-like molecules in fish reproduction. We found a direct action of leptin at the pituitary level on LH release using dispersed pituitary cells obtained from sea bass. The effect of leptin and its interaction with NPY on LH release in late prepubertal fish and those at the first spermiating stage suggests an important role of leptin as a regulator of the onset of puberty.

Because the initiation of puberty and the integrity of the reproductive function are physiologically coupled to nutritional status, it is logical to postulate that leptin, as a peripheral signal, and NPY play important roles in relaying information about energetic status to the reproductive axis in fishes as well as in mammals. However, this hypothesis depends on demonstration of the existence of leptin in fishes, which is supported by a preponderance of data. Future experiments will focus on the characterization of leptin in fishes. These findings provide a framework for an understanding of neuroendocrine mechanisms and the metabolic regulation of puberty and adult reproductive function.

ACKNOWLEDGMENTS

We are grateful to J. Ramos for collaboration on fish sampling, A. Forniés for help with the cell culture experiments, and Dr. F. Prat for his critical comments on this manuscript. We also thank Dr. J.M. Cerdá-Reverter for helpful discussion and for his valuable suggestions on the manuscript.

FOOTNOTES

First decision: 21 May 2001.

1 This work was supported by Ministerio de Educacion y Ciencia (MEC) of Spain (grant SB 99 CE 013361) and by European Union (EU) (MCFI-1999-01471). Back

2 Correspondence. FAX: 34 964 319 509;carrillo{at}iats.csic.es Back

Accepted: June 28, 2001.

Received: April 20, 2001.

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