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Nitric Oxide Modulation of the Dopaminergic Nigrostriatal System: Focus on Nicotine Action

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The Basal Ganglia IX

Part of the book series: Advances in Behavioral Biology ((ABBI,volume 58))

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Abstract

Nitric oxide (NO) signalling plays an important role in the integration of information processed by the basal ganglia nuclei. Accordingly, considerable evidence has emerged indicating a role for NO in pathophysiological conditions such as Parkinson’s disease (PD), schizophrenia and drug addiction. To further investigate the NO modulation of dopaminergic function in the basal ganglia circuitry, in this study we used in vivo electrophysiology and microdialysis in freely-moving rats. Pharmacological manipulation of the NO system did not cause any significant changes either in the basal firing rate and bursting activity of the dopamine (DA) neurons in the substantia nigra pars compacta (SNc) or in DA release in the striatum. In contrast, the disruption of endogenous NO tone was able to counteract the phasic dopaminergic activation induced by nicotine treatment in both experimental approaches. These results further support the possibility that nicotine acts via a NO mechanism and suggest a possible state-dependent facilitatory control of NO on the nigrostriatal DA pathway. Thus, NO selectively modulates the DA exocytosis associated with increased DA functiov n.

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References

  • Arnold WP, Mittal CK, Katsuki S and Murad F (1977) Nitric oxide activates guanylate cyclase and increases guanosine 3′:5′-cyclic monophosphate levels in various tissue preparations. Proc Natl Acad Sci USA 74: 3203–3207.

    Article  CAS  PubMed  Google Scholar 

  • Bernácer J, Prensa L and Giménez-Amaya JM (2005) Morphological features, distribution and compartmental organization of the nicotinamide adenine dinucleotide phosphate reduced-diaphorase interneurons in the human striatum. J Comp Neurol 489: 311–327.

    Article  PubMed  Google Scholar 

  • Bian K and Murad F (2003) Nitric oxide (NO)-biogeneration, regulation, and relevance to human diseases. Front Biosci 8: 264–278

    Article  Google Scholar 

  • Bredt DS, Hwang PM and Snyder SH (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347: 768–770.

    Article  CAS  PubMed  Google Scholar 

  • Campos F, Alfonso M, Vidal L, Faro LR and Durán R (2006) Mediation of glutamatergic receptors and nitric oxide on striatal dopamine release evoked by anatoxin-a. An in vivo microdialysis study. Eur J Pharmacol 548: 90–98.

    Article  CAS  PubMed  Google Scholar 

  • Choi YB and Lipton SA (2000) Redox modulation of the NMDA receptor. Cell Mol Life Sci 57: 1535–1541.

    Article  CAS  PubMed  Google Scholar 

  • Cox BA and Johnson SW (1998) Nitric oxide facilitates N-methyl-d-aspartate-induced burst firing in dopamine neurons from rat midbrain slices. Neurosci Lett 255: 131–134.

    Article  CAS  PubMed  Google Scholar 

  • Dawson VL and Dawson TM (1998) Nitric oxide in neurodegeneration. Prog Brain Res 118: 215–229

    Article  CAS  PubMed  Google Scholar 

  • Del Bel EA and Guimarães FS (2000) Sub-chronic inhibition of nitric-oxide synthesis modifies haloperidol-induced catalepsy and the number of NADPH-diaphorase neurons in mice. Psychopharmacology 147: 356–361.

    Article  PubMed  Google Scholar 

  • Del Bel EA, Bermúdez-Echeverry M, Salum C and Raisman-Vozari R (2007) Nitric oxide system and basal ganglia physiopathology. In: Di Giovanni G (ed) The Basal Ganglia Pathophysiology: Recent Advances. Transworld Research Network, Kerala, India, pp. 129–158.

    Google Scholar 

  • De Vente J, Markerink-van Ittersum M, van Abeelen J, Emson PC, Axer H and Steinbusch HW (2000) NO-mediated cGMP synthesis in cholinergic neurons in the rat forebrain: effects of lesioning dopaminergic or serotonergic pathways on nNOS and cGMP synthesis. Eur J Neurosci 12: 507–519.

    Article  PubMed  Google Scholar 

  • Dhir A and Kulkarni SK (2007) Involvement of nitric oxide (NO) signaling pathway in the antidepressant action of bupropion, a dopamine reuptake inhibitor. Eur J Pharmacol 568: 177–185.

    Article  CAS  PubMed  Google Scholar 

  • Di Giovanni G, De Deurwaerdére P, Di Mascio M, Di Matteo V, Esposito E and Spampinato U (1999) Selective blockade of serotonin-2C/2B receptors enhances mesolimbic and mesostriatal dopaminergic function: a combined in vivo electrophysiological and microdialysis study. Neuroscience 91: 587–597.

    Article  PubMed  Google Scholar 

  • Di Giovanni G, Ferraro G, Sardo P Galati S, Esposito E and La Grutta V (2003) Nitric oxide modulates striatal neuronal activity via soluble guanylyl cyclase: an in vivo microiontophoretic study in rats. Synapse 48: 100–107.

    Article  PubMed  Google Scholar 

  • Di Giovanni G, Ferraro G, Sardo P, Di Maio R, Carletti F and La Grutta V (2006) Microiontophoretic evidence that nitric oxide alters spontaneous activity of the substantia nigra pars reticulata neurons in the rat. Acta Physiol 188 (Suppl 652): P184.

    Google Scholar 

  • Di Matteo V, Benigno A, Pierucci M, Giuliano DA, Crescimanno G, Esposito E and Di Giovanni G (2006) 7-Nitroindazole protects striatal dopaminergic neurons against MPP+-induced degeneration: an in vivo microdialysis study. Ann N Y Acad Sci 1089: 462–471.

    Article  PubMed  Google Scholar 

  • Di Matteo V, Pierucci M, Di Giovanni G Benigno A and Esposito E (2007) The neurobiological bases for the pharmacotherapy of nicotine addiction. Curr Pharm Des 13: 1269–1284.

    Article  PubMed  Google Scholar 

  • Di Matteo V, Pierucci M, Benigno A, Crescimanno G, Esposito E and Di Giovanni G (2009) Involvement of nitric oxide in 6-OHDA-induced neurodegeneration: an ex vivo study. Ann NY Acad Sci 1155: 309–315.

    Google Scholar 

  • Duncan JA and Heales RJS (2005) Nitric oxide and neurological disorders. Mol Aspects Med 26: 67–96.

    Article  CAS  PubMed  Google Scholar 

  • Egberongbe YI, Gentleman SM, Falkai P, Bogerts B, Polak JM and Roberts GW (1994) The distribution of nitric oxide synthase immunoreactivity in the human brain. Neuroscience 59: 561–578.

    Article  CAS  PubMed  Google Scholar 

  • Esposito E, Di Matteo V and Di Giovanni G (2007) Death in the substantia nigra: a motor tragedy. Expert Rev Neurother 7: 7677–7697.

    Article  Google Scholar 

  • Eve DJ, Nisbet AP, Kingsbury AE, Hewson EL, Daniel SE, Lees AJ, Marsden CD and Foster OJ (1998) Basal ganglia neuronal nitric oxide synthase mRNA expression in Parkinson’s disease. Brain Res Mol Brain Res 63: 62–71.

    Article  CAS  PubMed  Google Scholar 

  • Fricchione G and Stefano GB (2005) Placebo neural systems: nitric oxide, morphine and the dopamine brain reward and motivation circuitries. Med Sci Monit 11: 54–65.

    Google Scholar 

  • Furchgott RF and Zawadski J (1980) The obligatory role of the endothelium in the relaxation of arterial smooth-muscle by acetylcholine. Nature 288: 373–376.

    Article  CAS  PubMed  Google Scholar 

  • Garthwaite J and Boulton CL (1995) Nitric oxide signalling in the central nervous system. Annu Rev Physiol 57: 683–706.

    Article  CAS  PubMed  Google Scholar 

  • Gomes MZ and Del Bel EA (2003) Effects of electrolytic and 6-hydroxydopamine lesions of rat nigrostriatal pathway on nitric oxide synthase and nicotinamide adenine dinucleotide phosphate diaphorase. Brain Res Bull 62: 107–115.

    Article  CAS  PubMed  Google Scholar 

  • González-Hernández T and Rodríguez M (2000) Compartmental organization and chemical profile of dopaminergic and GABAergic neurons in the substantia nigra of the rat. J Comp Neurol 421: 107–135.

    Article  PubMed  Google Scholar 

  • Govsa F and Kayalioglu G (1999) Relationship between nicotinamide adenine dinucleotide phosphate-diaphorase-reactive neurons and blood vessels in basal ganglia. Neuroscience 93: 1335–1337.

    Article  CAS  PubMed  Google Scholar 

  • Hunot S, Boissière F, Faucheux B, Brugg B, Mouatt-Prigent A, Agid Y and Hirsch EC (1996) Nitric oxide synthase and neuronal vulnerability in Parkinson’s disease. Neuroscience 72: 355–363.

    Article  CAS  PubMed  Google Scholar 

  • Johannes S, Reif A, Senitz D, Riederer P and Lauer M (2003) NADPH-diaphorase staining reveals new types of interneurons in human putamen. Brain Res 980: 92–99.

    Article  CAS  PubMed  Google Scholar 

  • Johnson MD and Ma PM (1993) Localization of NADPH diaphorase activity in monoaminergic neurons of the rat brain. J Comp Neurol 332: 391–406.

    Article  CAS  PubMed  Google Scholar 

  • Leontovich TA, Mukhina YK and Fedorov AA (2004) Neurons of the basal ganglia of the human brain (striatum and basolateral amygdala) expressing the enzyme NADPH-d. Neurosci Behav Physiol 34: 277–286.

    Article  CAS  PubMed  Google Scholar 

  • Nisbet AP, Foster OJ, Kingsbury A, Lees AJ and Marsden CD (1994) Nitric oxide synthase mRNA expression in human subthalamic nucleus, striatum and globus pallidus: implications for basal ganglia function. Brain Res Mol Brain Res 22: 329–332.

    Article  CAS  PubMed  Google Scholar 

  • Nowak P, Brus R, Oświecimska J, Sokoła A and Kostrzewa RM (2002) 7-Nitroindazole enhances amphetamine-evoked dopamine release in rat striatum. An in vivo microdialysis and voltammetric study. J Physiol Pharmacol 53: 251–263.

    CAS  PubMed  Google Scholar 

  • Sammut S, Dec A, Mitchell D, Linardakis J, Ortiguela M and West AR (2006) Phasic dopaminergic transmission increases NO efflux in the rat dorsal striatum via a neuronal NOS and a dopamine D(1/5) receptor-dependent mechanism. Neuropsychopharmacology 31: 493–505.

    Article  CAS  PubMed  Google Scholar 

  • Sammut S, Bray KE and West AR (2007) Dopamine D2 receptor-dependent modulation of striatal NO synthase activity. Psychopharmacology 191: 793–803.

    Article  CAS  PubMed  Google Scholar 

  • Sancesario G, Giorgi M, D’Angelo V, Modica A, Martorana A, Morello M, Bengtson CP and Bernardi G (2004) Down-regulation of nitrergic transmission in the rat striatum after chronic nigrostriatal deafferentation. Eur J Neurosci 20: 989–1000.

    Article  PubMed  Google Scholar 

  • Schilström B, Mameli-Engvall M, Rawal N, Grillner P, Jardemark K and Svensson TH (2004) Nitric oxide is involved in nicotine-induced burst firing of rat ventral tegmental area dopamine neurons. Neuroscience 125: 957–964.

    Article  PubMed  Google Scholar 

  • Tayfun Uzbay I and Oglesby MW (2001) Nitric oxide and substance dependence. Neurosci Biobehav Rev 25: 43–52.

    Article  CAS  PubMed  Google Scholar 

  • Vincent SR and Kimura H (1992) Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46: 755–784.

    Article  CAS  PubMed  Google Scholar 

  • West AR and Grace AA (2000) Striatal nitric oxide signalling regulates the neuronal activity of midbrain dopamine neurons in vivo. J Neurophysiol 83: 1796–1808.

    CAS  PubMed  Google Scholar 

  • West AR, Galloway MP and Grace AA (2002) Regulation of striatal dopamine neurotransmission by nitric oxide: effector pathways and signalling mechanisms. Synapse 44: 227–245.

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Dawson VL and Dawson TM (2006) Role of nitric oxide in Parkinson’s disease. Pharmacol Ther 109: 33–41.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported in part by Ateneo di Palermo research funding project ORPA068JJ5 (coordinator G. Di Giovanni).

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Authors and Affiliations

  1. Istituto di Ricerche Farmacologiche “MArio Negri”, Consorzio Mario Negri Sud, S. Maria Imbaro (Ch), Italy

    Vincenzo Di Matteo, Massimo Pierucci, Ennio Esposito, Giuseppe Crescimanno & Maurizio Casarrubea

  2. Dipartimento di Medicina Sperimentale, Sezione di Fisiologia Umana, “G. Pagano,” Università degli Studi di Palermo, Corso Tuköry 129, 90134, Palermo, Italy

    Arcangelo Benigno & Giuse Di Giovanni

Authors
  1. Vincenzo Di Matteo
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  2. Massimo Pierucci
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  3. Arcangelo Benigno
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  4. Ennio Esposito
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  5. Giuseppe Crescimanno
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  6. Maurizio Casarrubea
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  7. Giuse Di Giovanni
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Corresponding author

Correspondence to Giuse Di Giovanni .

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Editors and Affiliations

  1. Dept. Anatomy & Neurosciences, Vrije Universiteit Amsterdam, Amsterdam, 1007 MB, Netherlands

    Hendrik Jan Groenewegen

  2. Medical Center, Vrije Universiteit, Van der Boechorststraat 7, Amsterdam, 1081 BT, Netherlands

    Pieter Voorn

  3. Department of Neurology, Vrije Universiteit Medical Center, De Boelelaan 1117, Amsterdam, 1081 HV, Netherlands

    Henk W. Berendse

  4. Medical Center, Vrije Universiteit, Van der Boechorststraat 7, Amsterdam, 1081 BT, Netherlands

    Antonius B. Mulder

  5. Medical Centre, Radboud University Nijmegen, Geert Grooteplein 21a, Nijmegen, 6525 EZ, Netherlands

    Alexander R. Cools

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Matteo, V.D. et al. (2009). Nitric Oxide Modulation of the Dopaminergic Nigrostriatal System: Focus on Nicotine Action. In: Groenewegen, H., Voorn, P., Berendse, H., Mulder, A., Cools, A. (eds) The Basal Ganglia IX. Advances in Behavioral Biology, vol 58. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-0340-2_24

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  • DOI: https://doi.org/10.1007/978-1-4419-0340-2_24

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  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4419-0339-6

  • Online ISBN: 978-1-4419-0340-2

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