The Pineal Gland of Fishes

Amita Sarkar and Bhavna Upadhyay

Department of Zoology

Agra College, Agra (India) 282001

Abstract

The pineal gland is part of the endocrine system involved with rhythmic activity in e.g. fish. The main product of the pineal gland is the indole hormone melatonin, synthesised from the amino acid tryptophan. Melatonin is mainly synthesized when it is dark, as light inhibits production. For this reason melatonin is thought to be strongly involved in biological rhythms. The pineal gland is a photoneuroendocrine gland which secretes the hormone melatonin and conveys information to the brain via neural pathway. In fish the entire system (the photodetector, the circadian clock and melatonin synthesizing enzymes) is located in the pineal organ. Several experimental studies indicated that the pineal organ is able to translate environmental information (photoperiod and temperature) into rhythmic messages and the pineal hormone melatonin is the internal chemical messenger of environmental signal or Zeitgeber and controls a number of functions, especially reproduction, in vertebrates.

The pineal gland is considered to be part of the system regulating biological rhythmicity, mainly due to its main secretory product, the indole hormone melatonin [1]. In birds and mammals melatonin is strongly involved in the synchronization of diurnal and annual rhythms.

The pineal organ consists of the pineal gland and the parapineal organ. The parapineal organ is present in embryologic stages of development but is lacking in adult fish [2][3]. Whereas the role of melatonin in fish is less clear [4]. Three types of cells are considered the main content of the pineal gland, i.e. pinealocytes (photoreceptor cells), glial (supporting) cells and second order neurons (ganglion cells; [1][2]. There are blood vessels supplying blood to all parts of the pineal gland, but they do not penetrate into the parenchyma of the gland [5][6]. The pinealocytes are both photosensitive, containing photopigments, and secretory, producing chemical substances. Pinealocytes have been shown to undergo morphological changes in response to changes in photoperiod [2][3][7].

The photoreceptors of the pinealocytes have similarities with the cone photoreceptors of the retina [4]. They differ, however, as the time it takes for a resting membrane potential (the dark potential) in the individual pineal photoreceptors to reach peakpotential (hyperpolarizrtion) and the recovery time (the return to the resting potential after a stimulus) is much longer in the pineal gland than in the retina[8]). This supports the theory that the pineal gland records gradual light intensity changes rather than the rapid changes that the retina can perceive [7]. Further, the pineal pigments absorb light at longer wavelengths than the retina [9]. Photoreceptors of lower vertebrates presumably release neurotransmitters constantly during darkness[2], and the size and numbers of synaptic ribbons (part of the photoreceptor axon terminal) change with time of day and ambient light [10].

Melatonin (N-acetyl-5-methoxytryptamine) is an indole hormone produced from the amino acid tryptophan. The biosynthesis of melatonin starts with conversion of tryptophan into 5-hydroxytryptophan by the enzyme tryptophan hydroxylase (TPOH). Hydroxytryptophan is then decarboxylated by the aromatic amino acid decarboxylase to serotonin. Arylalkylamine N-acetyltransferase (AANAT) converts serotonin into Nacetylserotonin and hydroxyindole-0-methyltransferase (HIOMT) methylates Nacetylserotonin to melatonin [11].

The pineal gland is the main organ for melatonin production in fish, but there is melatonin production in the retina of the eye as well [10]. In mammals and birds melatonin is also produced in the gastrointestinal tract, and under specific nutrition-dependent circumstances this production may contribute to the levels of circulating melatonin, albeit not in a rhythmical fashion [5][12]. No consistent information has been found for melatonin production outside the retina and pineal gland in fish [13] but pinealectomized trout have shown increased mid-scotophase plasma melatonin level [14][15] found that pinealectomy in goldfish did not completely abolish plasma melatonin levels. The production from the retina is considered to be mainly for local (paracrine) use and is not in phase with the plasma melatonin level [12].

In fish the melatonin diffuses into the blood stream directly after the synthesis. Melatonin is believed to be involved in behavioural, physiological and biochemical rhythmic activity. An indication of this is the diurnal variations in indole compounds (serotonin, 5-hydroxyindolacetic acid, 5-hydroxytryptophol and melatonin) in the pineal and that the melatonin levels are consistently higher during night time [11][12]. Light inhibits the production of melatonin, while darkness removes this inhibition. The limiting factor is AANAT, which show cyclic activity with higher activity in darkness (in pike, Exos lucius, [11] Abundance of AANAT messenger RNA transcripts varies in a manner parallel to the enzyme activity [12]. Both the duration of the elevated nighttime level and the amplitude of plasma melatonin rhythm change in a fashion consistent with the seasonal change in photoperiod [15] providing calendar information to the animal. It has been shown that Arctic charr maintains diel and seasonal melatonin rhythm perfectly reflecting the daylength even in lakes covered by ice and snow [14].

A very high night-time plasma melatonin level was recorded in these fish in September, when the lake temperature was high (~10°C), whereas in June when there is constant light at high latitudes the 24 hour plasma melatonin levels in Arctic charr were constantly under the detection limit of the assay. Diel fluctuations of pineal melatonin production have also been described in species closely related to the Arctic charr such as rainbow trout (Oncorhynchus mykiss; [16] and Atlantic salmon [17] as well as in many other fish[4]. Portar, with his associates in 1995 and 1996 reported that melatonin levels decrease in pinealectomized fish. It was demonstrated that the pineal gland was the only organ in fish, responsible for the presence of melatonin in the blood and the level oscillated regularly over 24 hours showing low values during day and high over night [18]. A pineal control of gonadal maturation has been shown in fishes either by pinealectomy [19]. The above authors have reported the relation between pineal gland and melatonin with reproduction. The pineal gland controls reproduction through secretion of its hormone melatonin through pineal-hypophysispituitary-gonadal axis. Administration of melatonin inhibits the stimulatory effect of a long photoperiod and high temperature on the ovary in early preparatory phase. Treatment with melatonin during preparatory phase resulted in decreased ovarian weight and arrested ovarian recrudescence [20]. When the goldfishes were pinealectomized in spring and exposed to long photoperiod conditions, the ovaries regressed and plasma gonadotropin levels were significantely depressed compared to sham operated animals. Sham operated goldfish exposed to short photoperiod conditions in spring had regressing ovaries whereas pinealectomized animals under this regime either spawned or had ovaries in the late vitellogenic phase [18].

Several authors reported that gonadal function (wt. and histology) are inhibited with the administration of melatonin. It appears that pineal gland and melatonin are having inhibitory effect to thyroid hormone in fishes during gonadal development and maturation [21] which is specially required for the sex steroidogenesis in the process of reproduction. The pineal gland regulates carbohydrate metabolism by altering insulin responsiveness in the animal like goldfish[16]. Pinealectomy in this species causes a decrease in liver glycogen stores and disappearance in plasma glucose. These effects occur independently of photoperiod acclimation and are seasonal in nature. The hormone from this gland was observed having a h5^ oglycemic effect in the above species [21]. Several authors have reported that this gland and its hormone have a role to play in the colour change mechanism in fishes [22].

Melatonin is important in controlling the reproductive seasonality by stimulating the final stages of sexual maturation and by synchronizing the oocytematurity with optimal timing of spawning.[20] Melatonin has also been found to affect estradiol levels in mature carp females and to indirectly influence the GtH II secretion via hypothalamic stimulatory (GnRH) centers [22].

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