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Dopamine Receptor Agonists Regulate Levels of the Serotonin 5=HT, Receptor and Its Mrna in a Subpopulation of Rat Striatal Neurons

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Dopamine Receptor Agonists Regulate Levels of the Serotonin 5=HT, Receptor and Its Mrna in a Subpopulation of Rat Striatal Neurons The Journal of Neuroscience, June 1, 1996, 16(11):3727-3736 Dopamine Receptor Agonists Regulate Levels of the Serotonin 5=HT, Receptor and its mRNA in a Subpopulation of Rat Striatal Neurons Nathalie Laprade,’ Fatiha Radja,* Tom& A. Reader,233 and Jean-Jacques Soghomonianl 1Centre de Recherche en Neurobiologie and Dkpat-tement d’Anatomie, Fault6 de Mgdecine, Universitb Lava/, Quebec, Canada, and Dkpartements de *Physiologic et 3Psychiatrie, Facultk de Mkdecine, Universit6 de Mont&al, Quebec, Canada The effects of dopamine receptor agonists on the levels of the neurons after double-labeling of sections with a 5-HT,, and a striatal serotonin 5-HT,, receptor and its mRNA were investi- preproenkephalin (PPE) cRNA probe. In control unlesioned rats, gated in rats lesioned with 6-OHDA as neonates. The mRNA 5-HT,, mRNA labeling was distributed in PPE-labeled as well encoding for the .5-HT,, receptor was detected by in situ as in PPE-unlabeled striatal neurons. In 6-OHDA-lesioned rats, hybridization histochemistry and the binding to 5HT,, recep- increased 5-HT,, mRNA labeling was found only in PPE- tors was revealed with [‘251](2,5-dimethoxy-4-iodophenyl)2- unlabeled neurons and it was abolished after apomorphine or aminopropane ([‘251]DOI). In adult control unlesioned rats, la- SKF-38393 administration. These results demonstrate that beling with the 5-HT,, cRNA probe and with [‘251]DOI was agonists of dopamine receptors inhibit the expression of concentrated in medial sectors of the striatum. In 6-OHDA- 5-HT,, receptors in a subpopulation of presumed striato-nigral lesioned rats, labeling with the 5-HT,, cRNA probe or with neurons. We propose that this regulation plays an important [‘251]DOI was increased in the striatum, particularly in its lateral role in the control of motor activity by dopamine and 5-HT in the subdivisions. These increases were abolished after chronic basal ganglia. systemic administration of the dopamine receptor agonists apomorphine or SKF-38393. The mRNA levels encoding for the Key words: striatum; 5-HT; dopamine; 6-OHDA; 5-HT,, se- 5-HT,, receptor were further measured in individual striatal rotonin receptor; Dl dopamine receptor Dopamine and 5-HT play an important role in several brain puts to the striatum is also evidenced in adult rats injected with functions. Altered regulation of these two nemotransmitters in 6-OHDA as neonates. These rats demonstrate an important de- the basal ganglia is associated with various behavioral dysfunc- crease in the number of dopaminergic afferents and, at the same tions including motor and obsessive-compulsive disorders time, an increased density of 5-HT axons in the striatum, predom- (Sandyk et al., 1988). The striatum, one of the major components inantly in its rostra1 half (Stachowiak et al., 1984; Berger et al., of the basal ganglia, receives a dense dopaminergic input from the 1985; Snyder et al., 1986; Descarries et al., 1992). The S-HT substantia nigra pars compacta as well as serotoninergic projec- hyperinnervation is paralleled by an increase in striatal 5-HT tions from the dorsal raphe nucleus. Serotoninergic and dopa- content and reuptake (Luthman et al., 1987; Molina-Holgado et minergic systems in the striatum interact with each other, and al., 1993, 1994). Neonatal 6-OHDA lesions also induce an in- such interaction might play a key role in their respective modes of creased ligand binding to striatal serotonin S-HT,,,, 5-HT,,,,,,,An, action. For instance, it has been demonstrated that 5-HT facili- and 5-HT,, receptors (Radja et al., 1993) and an increased tates the release of dopamine in the striatum (Benloucif et al., responsiveness of striatal neurons to iontophoretic application of 1993; Gallaway et al., 1993; Yadid et al., 1994; Bonhomme et al., 5-HT receptor agonists (El Mansari et al., 1994). An increase in 1995) and regulates the firing rate of dopamine neurons in the 5-HT,,, but not 5-HT,, or 5-HT,,- (also called S-HT,(.), mRNA substantia nigra (Kelland et al., 1990). Reciprocally, dopamine levels has also been recently reported in the striatum of rats afferents are able to facilitate the release of 5-HT in the raphe injected with 6-OHDA as adults (Numan et al., 1995). dorsalis and, at the same time, inhibit this release in the striatum Adult rats lesioned with 6-OHDA as neonates demonstrate (Lee and Geyer, 1984; Ferre and Artigas, 1993; FerrC et al., 1994). supersensitive behavioral responses to the administration of do- An interaction between dopaminergic and serotoninergic in- pamine Dl receptor agonists (Breese et al., 1985a,b). In addition, the motor hyperactivity exhibited by these rats under drug-free conditions has been shown to involve 5-HT,, receptors (Luthman Received Jan. 19, 1996; revised March 6, lYY6; accepted March 8, 1996. The studies were funded by the Parkinson Foundation of Canada, the Natural et al., 1991). These data indicate that both the Dl and 5-HT,, Sciences and Engineering Research Council, and the Fonds de Recherche en SantC receptor subtypes are preferentially involved in some of the motor du Quibec (FRSQ) to J.-J& and by the Medical Research Council of Canada abnormalities and adaptive changes exhibited by rats lesioned (MTl2966) and the FRSQ to T.A.R. We thank Dr. D. Pritchett for the gift of the 5-HTzA receptor cDNA and Ms. G. Audet and Ms. I. Deaudelin for their expert with 6-OHDA as neonates. In the present study, we tested the technical assistance. hypothesis that dopamine receptor agonists, particularly Dl ago- Correspondence should be addressed to Dr. Jean-Jacques Soghomonian, Centre nists, are involved in the modulation of striatal 5-HT2, receptor de Recherche en Neurobiologic, HBpital de I’Enfant-JCsus, 1401 18 Rut, Quebec, Canada GIJ 124. levels in adult rats lesioned with 6-OHDA as neonates. Because Copyright 0 1996 Society for Ncuroscicnce 0270.6474/96/163727-10$05.00/O striatal projection neurons can be distinguished as two subpopu- 3728 J. Neurosci., June 1, 1996, 16(11):3727-3736 Laprade et al. l 5-I-IT,, Receptor Regulation by Dopamine lations that either express or do not express the preproenkephalin and 50 mgiml X-phosphate (all these chemicals were purchased from (PPE) mRNA, we further analyzed the fate of the mRNA encod- Boehringer Mannheim). The reaction was stopped by dipping the slides in Tris buffer (10 mM; pH 8.0) containing I mM EDTA. Sections were ing for the SHT,, receptor in these two neuronal subpopulations. washed in 2X SSC for 15 min, quickly dipped in ammonium acetate (300 mM), rinsed in 70% ethanol, and air dried. Sections were first juxtaposed MATERIALS AND METHODS to Kodak X-OMAT-AR x-ray films for 21 d and then processed for emulsion radioautography. In that case, sections were dipped in the Neonu,ul 6-OHDA treatments. Three pregnant female Sprague-Dawley Amersham LM-1 nuclear emulsion, air dried, and stored at 4°C in rats (Charles River, Montreal) were housed individually with water and light-tight boxes in presence of desiccant. After 4-8 d of exposure, the dry food available ad libitum. Three days after delivery, each litter was emulsion radioautographs were developed in Kodak D-19 for 3.5 min at reduced to 12 pups. Twenty-five pups were given bilateral cerebroven- 14°C and mounted with Aquaperm mounting media (Fisher Scientific, tricular injections of the neurotoxin 6-OHDA (Sigma, St. Louis, MO) and Orangeburg, NY). 6 pups (sham-opcratcd) were injected with the vchiclc (0.9% sodium [“.‘I]DOI binding. The serotonin 5-HT ZA receptors were labeled with chloride and 1% ascorbic acid) under anesthesia with methoxyflurane [“‘I]DOI (DuPont, Billerica, MA, specific activity 2200 Ciimmol), ac- vapors. Pups were injected either with a total of 100 pg of 6-OHDA in 10 cording to Mengod’s modification (Mengod et al., 1990; Radja et al., ~1 (5 ~1 in each vcntriclc) or with 10 ~1 of vehicle (sham-operated). All 1993) of the protocol of McKenna et al. (1989). Briefly, the sections (20 animals were pretreated with the noradrenaline uptake inhibitor desipra- pm thick) wcrc preincubated at 25°C for 30 min in 50 nlM Tris-HCI buffer mine (25 mg/kg, s.c.) 45 min before surgery, in order to protect norad- (pH 7.4) containing 4 mM CaCl,, 0.1% ascorbic acid, and 0.1% bovine renergic neurons. serum. They were then incubated for 90 min in the same buffer containing Phurmacologicul treatments. Sixty days after the surgery, the sham- 200 PM [‘Z”I]DOl, in the presence of 30 nM of unlabeled 5-HT to block operated and six of the 6-OHDA-lcsioned rats were injected subcutane- ously with vehicle (0.02% acetic acid in 0.9% NaCI). The other 6-OHDA- 5-HT,,. sites. Nonspecific binding was determined in the presence of 4 lesioned rats wcrc subdivided in three groups of six or seven animals that mM cold unlabeled 5-HT. After incubation with the radioligand, the slides were injected subcutaneously with the mixed dopaminc DI/D2 rcccptor were washed in cold butfer (2x 10 min) and dried under a stream of cold agonist apomorphinc (5 mg/kg), the preferential dopaminc DI receptor air. Autoradiographs wcrc gcneratcd by juxtaposition of the slides to agonist SKF-383Y3 (I 2.5 mgikg), or SKF-38393 in combination with the autoradiographic film (Hyperfilm, Amersham, Arlington Heights, IL), dopaminc Dl rcccptor antagonist SCH-23390 (0.2 mgikg). All injections together with Microscalcs (Amersham); the exposure lasted 3 d. were given twice daily for IO d. Three hours after the last injection, all rats /.‘H/r?zuzindo/ /Grzdir~g. The density of dopaminc rcuptakc sites in the were killed by decapitation; their brains were quickly removed and kept striatum was measured by [‘HI mazindol binding, as previously reported frozen at -70°C.
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