Diurnal changes in the content of indoleamines, catecholamines, and methoxyindoles in the pineal gland of the Djungarian hamster (Phodopus mngorus): Effect ...
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Journal of Pineal Research ISSN 0742-3098
J Pineal Res 1996; 2/:7-14 Printed in the United Stares ofAmerica--all rights reserved
Diurnal changes in the content of indoleamines, catecholamines, and methoxyindoles in the pineal gland of the Djungarian hamster (Phodopus mngorus):Effect of photoperiod Miguez JM, Recio J, Vivien-Roels B, PCvet P. Diurnal changes in the content of indoleamines, catecholamines and methoxyindoles in the pineal gland of the Djungarian hamster (Phodopus sungorus): Effect of photoperiod. J. Pineal Res. 1996; 21 :7-14. 0 Munksgaard, Copenhagen Abstract: Previous studies in Syrian hamster have shown that the correlations between the daily fluctuations in the contents of pineal indoleamines and methoxyindoles are influenced by the photoperiod, and that dopamine may play a role in the regulation of pineal function. The present study investigated the 24 hour changes in the content of 5hydroxytryptophan (5-HTP), serotonin (5-HT), 5-hydroxyindoleacetic acid (5-HIAA), N-acetylserotonin (NAS), melatonin, 5-methoxytryptophol ( 5 MT), noradrenaline (NA), dopamine (DA), and 3,4-dihydroxyphenylacetic acid (DOPAC) in the pineal gland of female Djungarian hamsters exposed to long (LP; LD 16:8) or short (SP; LD 10:14)photoperiods for 10 weeks. Pronounced nocturnal increases of N-acetylserotonin and melatonin content were observed irrespective of the photoperiod regime. The content of 5-HT was markedly decreased during the first hour of the night in LP, which contrasted with the lack of changes in NAS and melatonin content at this time. In SP, an increased 5-HTP content and a less obvious decrease in 5-HT content was observed during the night, although melatonin and NAS content were even higher than in LP. Similar daily patterns as for 5-HT were observed in the 5-HT oxidative metabolites (5-HIAA and 5-MT). When considering values throughout the day, a poor correlation for 5-HT vs.. NAS and melatonin content was observed, which was particularly evident during the nighttime. These data indicate that the daily variation of pineal indoles may not only be dependent on changes in the Nacetyltransferase activity but also in other mechanisms regulating pinealocyte 5-HT availability. As previously reported in other species of hamster, pineal NA content did not show daily variations in LP conditions, although a nocturnal increase was detected in SP. In contrast, pronounced nocturnal increases were observed in the content of DA and its acid metabolite, DOPAC, irrespective of the photoperiod. These data indicate the existence of an increased dopaminergic turnover during the night and further support a role for DA in the regulation of melatonin synthesis and in the synchronization of the pineal functions.
Introduction
It is well known that the daily rhythmic secretion of the pineal methoxyindole, melatonin, conveys photoperiodic information to the organism and me-
Jesus M. Miguez,' Joaquin Recio,"' Berthe Vivien-Roels,' and Paul PBvet' 'CNRS-URA 1332, Neurobiologie des fonctions rythmiques et saisonnieres, Universite Louis Pasteur, Strasbourg, France and 'Department of Physiology, University of Cantabria, Spain
Key wards: pineal gland - melatonin indoleamines -catecholeamines - rhythms - Djungarian hamster Address reprint requests to Or. P Pevet, CNRS-URA 1332, Neurobiologie des Fonctions Rythmiques et Saisonnieres, Laboratoire de Zoologie, Universite Louis Pasteur 12, Rue de I'Universite, 67000, Strasbourg, France. Received January 8, 1996; accepted April 19, 1996.
diates the photoperiodic regulation of reproduction in many seasonal species [Reiter, 1980, 19911. Other methoxyindoles, such as 5-methoxytryptophol (5ML) or 5-methoxytryptamine (5-MT), may also play a role in the photic control of seasonal repro7
Miguez et al. duction [Pkvet, 19831, although their relevance is, at present, not clear. The details of the neural and biochemical events controlling melatonin synthesis have been extensively studied in the rat [Wurtman and Ozaki, 1978; Balemans, 1981; Klein et al., 1981; King and Steinlechner, 19851. Photic information reaches the pineal gland via a multineuronal pathway involving the retina, the suprachiasmatic nuclei, and the superior cervical ganglia [Klein and Moore, 19791. Postganglionic fibers terminating in the pineal gland regulate the circadian metabolism of indole constituents, leading to the nocturnal synthesis of melatonin. Nocturnally increased release of noradrenaline (NA) from the sympathetic terminals interacts with a and p pineal adrenoceptors and initiates a variety of subcellular reactions which, finally, increase pineal cyclic AMP and stimulate N-acetyltransferase (NAT) activity, the rate limiting enzyme in melatonin synthesis [Klein et al., 19831. The pineal gland accumulates large amounts of serotonin (5-HT), the precursor of melatonin biosynthesis [Quay, 19631. The high nocturnal activity of the NAT may explain the opposite daily variation in melatonin and 5-HT content, at least in the rat pineal gland IMefford et al., 1982; Champney et al., 1984; McNulty et al., 19861. However, in some seasonal species such as the Syrian hamster [Miguez et al., 19951, the Djungarian hamster [Lerchl and Schlatt, 19921, and the European hamster [PCvet et al., 19891, daily fluctuations of melatonin and 5-HT content are not well correlated, particularly during the 1ight:dark and dark:light transition phases. This fact supports the hypothesis that pineal 5-HT content is regulated by other factors and not solely by NAT activity. Alternative routes of 5-HT utilization, mainly the synthesis of other metabolites such as 5hydroxyindoleacetic acid (5-HIAA), 5-ML7 5-MT, and 5-hydroxytryptophol [Pevet et al., 1981; Balemans, 19831, as well as changes in 5-HT synthesis or release [Aloyo and Walker, 1987, Azekawa et al., 19911, could underlie these differences. However, the circadian variations of these 5-HT metabolic pathways [Skene et al., 1987; Raynaud and PCvet, 19911 and their role in regulating 5-HT content in the pineal gland of these species are poorly understood. The function of the Djungarian hamster pineal gland has been shown to be affected by exposure of the animals to varying periods of light and darkness. These studies concerned primarily the daily variation in melatonin production [Goldman et al., 1981; Hoffman, 1981; Yellon et al., 1982; Illnerova et al., 1983, 1984, Lerchl and Schlatt, 1992, 19931, while other indoleamines have merited less attention. Daily changes in the pineal content of NA, 8
dopamine (DA), and related metabolites were also reported in this species, although only from individual day/night points [Hermes et al., 19941. The present study, therefore, was undertaken to examine the 24-hour rhythm of several indoleamines, methoxyindoles, and catecholamines present in the pineal gland of the female Djungarian hamster, as well as their photoperiodic dependency. Material and methods Animals and treatments
Female Djungarian hamsters were born and raised in long photoperiod (LP, LD 16:8, lights on from 0400 hr to 2000 hr) and controlled temperature (22 k 2.C). Food and water were provided ad libitum. At the beginning of the experiment they ranged from 3 to 6 months in age and 36.6 f 0.6 g in body weight. Animals were grouped in groups of 6-8 per cage and half of them were transferred to short photoperiod (SP; LD 10:14, lights on from 0800 hr to 1800 hr); the others remained in LP. A dim red light was always present to allow manipulation during darkness, and animals had free access to food and water. Ten weeks later, five animals from each photoperiod were sacrificed without anesthesia at six time-points throughout the light-dark cycle (1 hour before and after lights on and off, and in the middle of the light and dark periods). After sacrifice, the sexual status of the animals was established by weighing uteri, and the pineal glands were dissected, frozen in liquid nitrogen and stored at -8O.C until assay. Sample preparation and HPLC analysis
The pineal content of 5-hydroxytryptophan (SHTP), 5-HT, 5-HIAA, N-acetylserotonin (NAS), NA, DA, and 3-4-dihydroxyphenylacetic acid (DOPAC) were analysed by a modification of the high performance liquid chromatographic method described by Adell et al. [ 19911. Single pineal glands were sonicated in 100 pl of a solution of 0.4 M perchloric acid containing 0.8 mM sodium metabisulfite and 0.1 mM EDTA. The suspension was centrifuged (14,000 rpm/2 minutes) and 10 p1 of the supernatant were diluted in 200 p1 of mobile phase and injected onto the chromatographic system. Mobile phase consisting of 0.1 M P04H2K, 0.7 mM octanesulfonic acid, 0.1 mM EDTA-Na2, and 18% methanol (pH final of 2.9 adjusted with phosphoric acid) was pumped (Model M590; Waters) to a flow rate of 0.8 ml/ minute through a reversed phase ultrasphere ODS C18 column (75 mm x 4.6 mm, 3 mm particle size; Beckman, San Ramon, CA), which was coupled to a Coulochem M5 1 OOA detector (ESA, Bedford,
Pineal amines and metabolites in Djungarian hamster
MA). The detection system included a guard cell (M5020) set at a potential of +lV and a double analytical cell (M501l ) maintained at +O.OSV (first cell) and +0.28V (second cell). The amines were oxidized under the second analytical cell and the signal was recorded on a Waters 740 Data module integrator. The limits of detection were between 1 and 3 pg/ 20 pi sample for the different compounds, with a signal noise ratio of two. Radioimmunoassays
Aliquots of 90 pl of hamster pineal homogenates were used for measurement of melatonin and 5-ML by radioimmunoassay, following extraction with dichloromethane according to the method of Brown et al. [ 19851. Melatonin was assayed by using a rabbit antiserum (R 19540, M A , Nouzilly, France) at a final dilution of 1/250,000and 2-[ 125I]-iodomelatonin. The limit of sensitivity of the assay, defined as two standard deviations of maximum binding, was 1.0 pg/tube. Usually the minimum detection levels for the assay were between 5 and 10 pg/pineal; 5-ML was measured following the assay developed by Skene et al. [ 19861, using a sheep antiserum (batch number 1320) at a final dilution of 1/80,000 and iodinated 5-ML. The limit of sensitivity of the assay, defined as two standard deviations of maximum binding, was 2.5 pg/tube. The assays were validated by parallelism studies. Pooled hamster pineal homogenates, serially diluted with assay buffer, gave parallel displacements to those of melatonin and 5-ML standards curve. Statistical analysis
One-way ANOVA followed by Student-NewmanKeuls test was used to assess differences among values at various times of day for each photoperiodic regime and between them. Two-way ANOVA was used to test whether the environmental lighting regime altered the diurnal variation of pineal compounds. Results
After 10 weeks in SP LD 10:14, the uterine weights of the animals showed a significant decrease as compared to those maintained in LP LD 1623 (LP: 0.149 k 0.013 g, SP: 0.071 k 0.003 g; P
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an increased tryptophan hydroxylase activity [Ehret et al., 19911. By contrast in the Syrian hamster tryptophan hydroxylase activity is higher during the day than during the night [Steinlechner et al., 1982; PCvet P., unpublished data], indicating perhaps a different enzyme regulation. Our present results in the Djungarian hamster show a higher 5-HTP and 5-HT pineal levels in SP than in LP, that suggests the existence of a greater nocturnal 5-HT synthesis in the former that could also be involved in maintaining a higher melatonin production. We do not, however, exclude the possibility of the existence of specific differences between 5-HT and melatonin turnover in the photoperiods underlying the lack of correlation between their contents. In the pineal gland, the two major metabolic routes for 5-HT are N-acetylation and oxidation [King and Steinlechner, 19851. This study shows that the diurnal variations of pineal oxidative metabolites, 5-HIAA and 5-ML, are opposite to those of NAS and melatonin. Moreover, the content of 5-HIAA and 5-ML displayed a high correlation with the concentration of 5-HT, indicating that the oxidative processes are not involved in regulating the diurnal rhythm of 5-HT in the pineal gland. Hence, their participation in the differences found between 5-HT and melatonin content in the pineal gland seem to be unlikely. To our knowledge, this is the first report describing diurnal variations of pineal 5-ML in the Djungarian hamster. Previous studies in Syrian hamster have shown a similar daily variation of 5-ML, despite of 5-10-fold higher levels [Skene et al., 1987; Miguez et al., 19951. In other species, such as the European hamster and the jerboa, the day-night variations in pineal 5-ML content were only seen
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F i g . 3. Diurnal changes of dopamine (DA), 3-4-dihydroxyphenylacetic acid (DOPAC), and noradrenaline (NA) contents in the pineal gland of Syrian hamsters kept in long (LD 16:08, LP) and short (LD 10: 14, SP) photoperiods. The solid bars indicate the periods of darkness. Values are mean f S.E.M. of 4-5 animals. * Pi0.05 as compared to daytime values.
in specific times of the year, pointing to a peculiar pattern of 5-ML production under certain photoperiodic conditions [Lakhdar-Ghazal et al., 1992;Vivien-Roels et al., 19921.Whether difference in 5-ML production among species has a physiological significance in relation to photoperiodic time measurement remains to be defined since to date no clear physiological function has been attributed to 5-ML [Reiter et al., 1975;Vaughan et al., 1976;PCvet, 19831. 12
Studies in the rat agree on the existence of a daily rhythm in pineal NA content with higher nocturnal amounts [Brownstein and Axelrod, 1974;Saavedra et al., 1982;Craft et al., 19841.This is not the case in the Syrian or the Djungarian hamster, in which no diurnal changes in NA content were found [Morgan and Reiter, 1976;Craft et al., 1984;Hermes et al., 1994;Miguez et al., 19951.Our present data also fail to detect a rhythm of NA content in LP exposed hamsters, although a nocturnal increase was found in SP. We also reported here a pronounced rhythmic pattern of pineal DA content, which was accompanied by a similar rhythmic fluctuation of its acid metabolite, DOPAC. These data suggest the existence of an increased synthesis and metabolism of catecholamines during the night, in agreement with previous reports in Syrian hamster [Craft et al., 19841.In contrast to NA, daily variations of DA and DOPAC were present in both LP and SP, suggesting the existence of photoperiod-dependent changes in the sympathetic neuronal activity affecting NA synthesis, release, or intraneuronal storage [Taylor and Wilson, 19701 that may contribute to the differences in content. Pineal DA levels increased by 300% during the night, and they were 3-5 times higher than those reported in the Syrian hamster [Miguez et al., 19951 and 2 times lowers than those of the rat [Fujiwara et al., 1980;Hermes et al., 19941.The inverse correlation between melatonin production and DA content in the pineal gland of these three species suggests a role for DA in the nocturnal pineal activation. Several other data from the literature support this view. For example, the administration of the DA precursor, 3-4-dihydroxyphenylalanine(LDOPA), is followed by an increased melatonin synthesis [Lynch et al., 19731.Dopamine has been also shown to increase NAT activity and melatonin production in vitro [Axelrod et al., 1972;Govitrapong et al., 19891,and dopaminergic receptors have been characterized in the mammalian pineal gland [Govitrapong, 1984; Simonneaux et al., 1990, 19911.Recent studies have also reported the existence of intrinsic dopaminergic cells in hamster and rat pineal gland [Hernandez et al., 1994; Hermes et al., 19941,indicating that additional sources may contribute to pineal DA levels. Our data agree with previous reports on the existence of an enhanced dopaminergic, and perhaps not noradrenergic, activity in the Djungarian hamster pineal gland during the night [Hermes et al., 19941,suggesting a double role of DA in the pineal, i.e., as a neurotransmitter and as a precursor to NA synthesis.
Pineal amines and metabolites in Djungarian hamster
Acknowledgments
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