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Relationships Between the Effects of Peripherally Administered Salmon Calcitonin on Calcaemia and Brain Biogenic Amines

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Relationships Between the Effects of Peripherally Administered Salmon Calcitonin on Calcaemia and Brain Biogenic Amines Relationships between the Effects of Peripherally Administered Salmon Calcitonin on Calcaemia and Brain Biogenic Amines Renato GAGGI, Rosaria DE IASIO and Anna Maria GIANNI Instituteof Pharmacology,University of Bologna,Via Irnerio 48, 40126 Bologna,Italy Accepted May18, 1989 Abstract-The effects of s.c. administered salmon calcitonin on the biogenic amine neurotransmitters and metabolites were studied in discrete brain sections in order to evaluate the relationships between these central effects and the fall of serum calcium and to investigate the mechanisms of calcitonin-induced behavioral changes. The biogenic amines and metabolites were simultaneously determined by high-performance liquid chromatography with electrochemical detection in tissue samples obtained from rats treated with 10-80 MRC U/kg of the peptide. Some rats were pretreated with calcium lactate to inhibit the calcitonin-induced hypo calcaemia. Most of the effects, consisting of signs of serotonergic system activation, have been observed in the hypothalamus, accounting for some behavioral effects of the peripherally administered salmon calcitonin. It was speculated that the acti vation of the brain serotonergic system could result from two indirect and separate mechanisms: the first, which would involve enhanced serotonin synthesis, seemed to be facilitated by calcium availability. A second possible mechanism, which would involve enhanced serotonin release from the neurons, seemed to be mediated by the fall of calcium levels in the blood. It is well-known (1, 2) that the peripheral clarified. However, s.c. administered sCT administration of salmon calcitonin (sCT) does not have any effect on body temperature induces an increase in the brain levels of (R. Gaggi, unpublished observation). In serotonin (5HT) and its metabolite 5-hy regard to its effects on the noxious stimuli droxyindole-3-acetic acid (5HIAA), which response, a single sCT injection is ineffective, may be explained by activation of the seroton whereas repeated s.c. administrations in the ergic systems. mouse induce hyperalgesia (12). On the other hand, the serotonergic sys In any case, it is likely that all the central tems play an important role in several func effects of peripherally administered sCT are tions of the central nervous system including induced by an indirect mechanism. In fact, the release of hormones from the hypophysis, there are no convincing data suggesting the sensitivity to noxious stimuli, as well as the idea that this peptide passes the blood-brain regulation of food intake, body temperature barrier. Since the centrally active doses of sCT and locomotor activity. 5HT agonists adminis are high enough to produce hypocalcaemia tered to rats induce head-twitch behavior (13), and neuronal function has been shown (3, 4). These facts are consistent with the (14, 15) to be sensitive to physiological observations that sCT influences the release changes in calcium concentration, it is likely of hormones from the hypophysis (5-8), in that some sCT effects are mediated by the fall duces anorexia (9), depresses the amphet of calcium levels in the blood. amine-induced locomotor activity (10) and In fact, relationships between the hypo potentiates the head-twitch behavior elicited calcaemic and anorectic effects of various by 5-hydroxytryptophan (11). Notwithstand calcitonins have been demonstrated (13). ing, the role of the serotonergic system ac Moreover, it has been hypothesized that the tivation in some of these effects should still be effects mediated by hypocalcaemia also in clude changes in the functional state of the dopamine (DA), serotonin (5HT), 5-hydroxy serotonergic system by which sCT poten indole-3-acetic acid (5HIAA), 3,4-dihydroxy tiates the head twitch response elicited by 5 benzylamine (DHBA) and octyl sulfate hydroxytryptophan (11). In this regard, it is sodium salt (OSA) were obtained from Sigma likely that many other neuronal systems, (St. Louis, MO, U.S.A.). Ascorbic acid and besides the serotonergic system, should be triethylamine were from Farmitalia (Milano, influenced by hypocalcaemia. This may con Italy) and methanol was from Inalco S.p.A. tribute to the central effects of sCT. (Milano, Italy). The other reagents were pro The aim of the present work was to in ducts of Merck (Darmstadt, F.R.G.). vestigate the effects of s.c. administered sCT Treatments: The rats were treated with sCT, on the biogenic amine neurotransmitters and by the subcutaneous route, and calcium its metabolites in discrete brain sections and lactate, by the intraperitoneal route, dissolved to evaluate the relationships between these in saline. The control animals received saline effects and the calcium levels in the serum. alone. Three experiments were performed. In the first experiment, 20 MRC U/kg of Materials and Methods sCT was administered to 5 groups of 4 rats Animals and general procedure: Male 8, 4, 2, 1 or 0.5 hr before the sacrifice. A con Sprague-Dawley rats (Nossan, Milano, Italy) trol group of 4 rats received saline 0.5 hr weighing 250-300 g were used. They were before the sacrifice. housed under controlled conditions of light In the second experiment, 10 groups of 4 (7:00 a.m.-7.00 p.m.), temperature (22±2°C) rats were treated with saline or sCT 10, 20, 40 and humidity (60%) with food and water ad and 80 MRC U/kg, 8 or 2 hr before the libitum. On the day of the experiment, all the sacrifice. rats were food deprived at 9:00 a.m. while For one part of the third experiment, 4 the water was kept ad libitum. All the rats groups of rats were used. The first two groups were sacrificed by means of decapitation in were treated with saline, while the third and the afternoon (4:00 p.m.-6:00 p.m.). A blood fourth groups received calcium lactate 100 or sample was collected and the brain of each 200 mg/kg. After 10 min, the first group animal rapidly removed and ice-cooled. The received saline, while the remaining 3 groups cerebellum and olfactory tubercles were were sCT-treated. All these rats were sacrific discarded, whereas the hypothalamus, hip ed 2 hr later. In the same day, another 4 pocampus, striatum, brainstem (pons plus groups of rats were treated in the same way, medulla oblongata) and cerebral cortex were but the calcium lactate dose for the third and dissected (16). Each sample was immediately the fourth group was 200 mg/kg. Four hours frozen with pulvered dry ice and kept at later, the same dose of the calcium salt was -25 °C until the time of analysis . The rem again administered to the fourth group; Thus nant cerebral tissue, consisting mostly of the the rats of this group received 400 mg/kg of thalamus and midbrain, was also collected calcium lactate (2 x 200 mg/kg at a 4 hr and frozen. In the present work, this brain interval). All these rats were sacrificed 8 hr section will henceforth be designated as the after the sCT administration. The dose of sCT "remnant" . was 20 MRC U/kg. The procedure was re Chemicals: Synthetic salmon calcitonin peated using 80 MRC U/kg of sCT. All (sCT) was kindly supplied by Sandoz together, 16 groups of 4 rats were used in the Farmaceutici S.p.A. (Milano, Italy) as com third experiment. mercial vials containing 100 MRC U=20,ug of Analytical procedures: The determination peptide, 2 mg of acetic acid, 2 mg of sodium of the calcium levels in rat serum was per acetate, 7.5 mg of sodium chloride and dis formed with a colorimetric method (Test tilled water to 1 ml volume. Calcium lactate combination Boehringer Mannheim GmbH, was obtained'from Fluka AG (Buchs, Switzer Mannheim, F.R.G.). The determinations of land). For the analytical procedure, norepi biogenic amines and its metabolites in the nephrine (NE), 3,4-d 1hydroxyphenyl -acetic brain sections were performed simultaneously acid (DOPAC), homovanillic acid (HVA), by high-performance liquid chromatography (HPLC) with electrochemical detection (17, 18). The HPLC system consisted of a P 330 Results pump (Violet, Roma, Italy) linked to a First experiment: Effects of the sCT ad Rheodyne 7125 injector. The column (OD51 ministered at the dose of 20 M RC U/kg during C18: 10 ,um, 25 cm x 4 mm i.d.) and the pre the 8 hr following treatment: As shown column (ODS1-C18: 10 ,um, 5 cm x 4 mm IA.) (Table 1), the treatment induced marked were also from Violet. The electrochemical hypocalcaemia (F(5,18)=5.85, P<0.01) that detector (Eldec 103; Chromatofield, Chateau reached its maximum in 30 min (t(5,18)= neuf-Les Martigues, France) was connected 4.00, P<0.01) and remained substantially with a TRIO integrator (Trivector Systems Int., unchanged during the whole period of obser Ltd., Sandy, England). The potential of the vation (after 8 hr: t(5,18)=4.63, P<0.01). glassy-carbon electrode versus silver-silver In regard to the levels of NE, DA, HVA and chloride reference electrode was maintained DOPAC (data not shown) in all the examined at +0.8 V. The mobile phase consisted of a brain sections, the sCT did not induce signifi 840:160 mixture of 0.1 M NaH2PO4 and cant changes with respect to control. On the methanol. The mixture was made 2.6.10-3 M other hand the levels of all these amines and in OSA, 1.0.10-4 M in EDTA and 2.5.10-4 M metabolites in the brain sections of the control in triethylamine, and the pH was adjusted to rats were in the normal range. The following 3.4 with 3 M H3 P04. The flow rate was 1.5 values were observed (the values in ,ag/g of ml/min.
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