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Muscarinic cholinergic receptor-mediated modulation on striatal c-fos mRNA expression induced by levodopa in rat brain

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Summary

To clarify the interactions between dopamine receptors and muscarinic cholinergic receptors by which neurotransmitters may affect genetic responses, we studied the effects of the muscarinic cholinergic agonist, carbachol, and the muscarinic cholinergic antagonist, trihexyphenidyl, on levodopa-induced c-fos messenger RNA (mRNA) expression in rat striatum. Animals were administered levodopa (levodopa with one-tenth dosage of carbidopa), carbachol or thrihexyphenidyl alone or administered in combination as levodopa (100 mg/kg) + carbachol, or levodopa + trihexyphenidyl given as a single bolus. Levodopa given alone increase the expression of c-fos mRNA. Although carbachol or trihexyphenidyl alone was ineffective in inducing c-fos mRNA, the combination of levodopa and carbachol (⩾ 0.1 mg/kg) significantly suppressed the induction of c-fos mRNA as compared with levodopa given alone. The combined administration of levodopa and trihexyphenidyl showed a trend toward an additive effect on the induction of c-fos mRNA vs levodopa alone. These findings suggest that the muscarinic cholinergic system may modulate the levodopa-induced c-fos mRNA expression which then regulates the expression of other mRNAs.

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References

  • Arenander AT, de Vellis J, Herschman HR (1989) Induction of c-fos and TIS genes in cultured rat astrocytes by neurotransmitters. J Neurosci Res 24: 107–114

    PubMed  Google Scholar 

  • Asanuma M, Ogawa N, Haba K, Hirata H, Mori A (1992 a) Effects of chronic catecholamine depletions on muscarinic M 1-receptor and its mRNA in rat brain. J Neurol Sci 110: 205–214

    PubMed  Google Scholar 

  • Asanuma M, Ogawa N, Hirata H, Haba K, Chou H, Mori A (1992 b) Late onset and long-lasting suppressive effects of ceruletide, an analogue of cholecystokinin on c-fos mRNA expresion in the rat striatum. Neurosci Lett 138: 233–236

    PubMed  Google Scholar 

  • Asanuma M, Ogawa N, Hirata H, Haba K, Chou H, Mori A (1992 c) Opposite effects of rough and gentle handling with repeated saline administration of c-fos mRNA expression. J Neural Transm [GenSect] 90: 163–170

    Google Scholar 

  • Bertorelli R, Consolo S (1990) D 1 and D 2 dopaminergic regulation of acetylcholine release from striata of freely moving rats. J Neurochem 54: 2145–2148

    PubMed  Google Scholar 

  • Campeacu S, Hayward MD, Hope BT, Rosen JB, Nestler EJ, Davis M (1991) Induction of the c-fos proto-oncogene in rat amygdala during unconditioned and conditioned fear. Brain Res 565: 349–352

    PubMed  Google Scholar 

  • Carlsson A, Lindqvist M (1963) Effect of chlorpromazine or haloperidol on formation of 3-methoxy-tyramine and normetanephrine in mouse brain. Acta Pharmacol Toxicol 20: 140–144

    Google Scholar 

  • Chang HT (1988) Dopamine-acetylcholine interaction in the rat striatum: a dual-labeling immunocytochemical study. Brain Res Bull 21: 295–304

    PubMed  Google Scholar 

  • Chang SL, Squinto SP, Harlan RE (1988) Morphine activation of c-fos expression in rat brain. Biochem Biophys Res Commun 157: 698–704

    PubMed  Google Scholar 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156–159

    Article  PubMed  Google Scholar 

  • Cole AJ, Bhat RV, Patt C, Worley PF, Baraban JM (1992) D1 dopamine receptor activation of multiple transcription factor genes in rat striatum. J Neurochem 58: 1420–1426

    PubMed  Google Scholar 

  • Curran T, Bravo R, Muller R (1985) Transient induction of c-fos and c-myc in an immediate consequences of growth factor stimulation. Cancer Surv 4: 655–681

    PubMed  Google Scholar 

  • Dragunow M, Robertson GS, Faull RLM, Robertson HA, Jansen K (1990) D2 dopamine receptor antagonists induced Fos and related proteins in rat striatal neurons. Neuroscience 37: 287–294

    PubMed  Google Scholar 

  • Glowinski J, Iversen LL (1966) Regional studies of catecholamines in the rat brain. I. The disposition of [3H]norepinephrine, [3H] dopamine and [3H]DOPA in various regions of the brain. J Neurochem 13: 655–669

    PubMed  Google Scholar 

  • Graybiel AM, Moratalla R, Robertson HA (1990) Amphetamine and cocaine induce drugspecific activation of the c-fos gene in striosome-matrix compartments and limbic subdivisions of the striatum. Proc Natl Acad Sci USA 87: 6912–6916

    PubMed  Google Scholar 

  • Greenberg ME, Ziff EB, Greene LA (1986) Stimulation of neuronal acetylcholine receptors induces rapid gene transcription. Science 234: 80–83

    PubMed  Google Scholar 

  • Gubits RM, Smith TM, Fairhurst JL, Yu H (1989) Adrenergic receptors mediate changes in c-fos mRNA levels in brain. Mol Brain Res 6: 39–45

    PubMed  Google Scholar 

  • Kebabian JW, Calne DB (1979) Multiple receptors for dopamine. Nature 277: 93–96

    PubMed  Google Scholar 

  • Lehmann J, Langer SZ (1983) The striatal cholinergic interneuron: synaptic target of dopaminergic terminals? Neuroscience 10: 1105–1120

    PubMed  Google Scholar 

  • Miller JC (1990) Induction of c-fos mRNA expression in the rat striatum by neuroleptic drugs. J Neurochem 54: 1453–1455

    PubMed  Google Scholar 

  • Miller JC, Stone EA, Filer D, Friedhoff AJ (1989) Induction of c-fos gene expression on rat cortex during stress. Soc Neurosci Abstr 15: 799

    Google Scholar 

  • Mizukawa K, Ogawa N, Sora YH (1988) Amine fluorescence histochemical investigation of the striatum in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced Parkinsonian mice. Res Commun Chem Pathol Pharmacol 59: 121–128

    PubMed  Google Scholar 

  • Morgan JI, Cohen DR, Hempstead JL, Curran T (1987) Mapping patterns of c-fos expression in the central neurvous system after seizure. Science 237: 192–197

    PubMed  Google Scholar 

  • Nakajima T, Daval JL, Gleiter CH, Deckert J, Post RM, Marangos PJ (1989 a) C-fos mRNA expression following electrical-induced seizure and acute nociceptive stress in mouse brain. Epilepsy Res 4: 156–159

    PubMed  Google Scholar 

  • Nakajima T, Daval JL, Morgan PF, Post RM, Marangos PJ (1989 b) Adenosinergic modulation of caffeine-induced c-fos mRNA expression in mouse brain. Brain Res 501: 307–314

    PubMed  Google Scholar 

  • Nguyen TV, Kosofsky BE, Birnbaum R, Cohen BM, Hyman SE (1992) Differentioa expression of c-Fos and Zif268 in rat striatum after haloperidol, clozapine, and amphetamine. Proc Natl Acad Sci USA 89: 4270–4274

    PubMed  Google Scholar 

  • Ogawa N, Sora HY, Sato H, Mizukawa K (1987) Reduction of muscarinic cholinergic receptors in mouse striatum by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine and its recovery by levodopa treatment. Res Commun Chem Pathol Pharmacol 57: 133–136

    PubMed  Google Scholar 

  • Onodera H, Kogure K, Ono Y, Igarashi K, Kiyota Y, Nagaoka A (1989) Proto-oncogene c-fos is transiently induced in the rat cerebral cortex after forebrain ischaemia. Neurosci Lett 98: 101–114

    PubMed  Google Scholar 

  • Pletscher A (1966) Pharmacological and biochemical basis of some somatic side effects of psychotropic drugs. Excerpta Medica, Amsterdam, p 571 (Int Congr Series 129)

    Google Scholar 

  • Pollack AE, Wooten GF (1992) D2 dopaminergic regulation of striatal preproenkephalin mRNA levels is mediated at least in part through cholinergic interneurons. Mol Brain Res 13: 35–41

    PubMed  Google Scholar 

  • Robertson GS, Herrera DG, Dragunow M, Robertson HA (1989) L-dopa activates c-fos in the striatum ipsilateral to a 6-hydroxydopamine lesion of the substantia nigra. Eur J Pharmacol 159: 99–100

    PubMed  Google Scholar 

  • Robertson GS, Vincent SR, Fibinger HC (1990) Striationigral projection neurons contain D1 dopamine receptor-activated c-fos. Brain Res 523: 288–90

    PubMed  Google Scholar 

  • Robertson HA, Peterson MR, Murphy K, Robertson GS (1989) D1-dopamine receptor agonists selectively activate striatal c-fos independent of rotational behaviour. Brain Res 503: 346–349

    PubMed  Google Scholar 

  • Rodbell M (1980) The role of hormone receptors and GTP-regulatory proteins in membrane transduction. Nature 284: 17–22

    PubMed  Google Scholar 

  • Scatton B (1982) Further evidence for the involvement of D2, but not D1 dopamine receptors in dopaminergic control of striatal cholinergic transmission. Life Sci 31: 2883–2890

    PubMed  Google Scholar 

  • Sharp FR, Sagar SM, Hicks K, Lowenstein D, Hisanaga K (1991) c-fos mRNA, Fos and Fos-related antigen induction by hypertonic saline and stress. J Neurosci 11: 12321–12331

    Google Scholar 

  • Stoof JC, De Boer T, Sminia P, Mulder AH (1982) Stimulation of D2-dopamine receptors in the rat neostriatum inhibits the release of acetylcholine and dopamine but does not affect the release of gamma-aminobutyric acid, glutamate or serotonin. Eur J Pharmacol 84: 211–214

    PubMed  Google Scholar 

  • Stoof JC, Verheijden PFHM, Leysen JE (1987) Stimulation of D2-receptors in rat nucleus accumbens slices inhibits dopamine and acetylcholine release but not cyclic AMP formation. Brain Res 423: 364–368

    PubMed  Google Scholar 

  • Szekely AM, Barbaccia ML, Costa E (1987) Activation of specific glutamate receptor subtypes increases c-fos proto-oncogene expression in primary cultures of neonatal rat cerebellar granule cells. Neuropharmacology 26: 1779–1782

    PubMed  Google Scholar 

  • Trejo J, Brown JH (1991) c-fos and c-jun are induced by muscarinic receptor activation of protein kinase C but are differentially regulated by intracellular calcium. J Biol Chem 266: 7876–7882

    PubMed  Google Scholar 

  • Young ST, Porrino LJ, Iadarola MJ (1991) Cocaine induces striatal c-fos-immunoreactive proteins via dopaminergic D1 receptors. Proc Natl Acad Sci USA 88: 1291–1295

    PubMed  Google Scholar 

  • Yu M, Mizobe F, Yamamoto T, Kato T (1989) Differential effects of M1 and M2 muscarinic drugs on striatal dopamine release and metabolism in freely moving rats. Brain Res 495: 232–242

    PubMed  Google Scholar 

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  1. H. Chou

    Present address: Department of Neuroscience, Institute of Molecular and Cellular Medicine, Okayama University Medical School, Okayama, Japan

Authors and Affiliations

  1. Department of Neuroscience, Institute of Molecular and Cellular Medicine, Okayama University Medical School, Okayama, Japan

    N. Ogawa, M. Asanuma, H. Hirata & A. Mori

  2. Third Department of Internal Medicine, Okayama University Medical School, Okayama, Japan

    H. Hirata

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  1. H. Chou
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  2. N. Ogawa
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  3. M. Asanuma
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  4. H. Hirata
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  5. A. Mori
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Chou, H., Ogawa, N., Asanuma, M. et al. Muscarinic cholinergic receptor-mediated modulation on striatal c-fos mRNA expression induced by levodopa in rat brain. J. Neural Transmission 90, 171–181 (1992). https://doi.org/10.1007/BF01250959

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  • DOI: https://doi.org/10.1007/BF01250959

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