The role of nitric oxide donors in schizophrenia: Basic studies and clinical applications

European Journal of Pharmacology

Volumn 766, Issue , 2015, Pages 106-113

  Pitsikas, Nikolaos ^a  

^a UNIVERSITY OF THESSALY   (Greece)

Author keywords

Nitric oxide; Nitric oxide donor; Schizophrenia

Indexed keywords

AMPHETAMINE; APOMORPHINE; CYCLIC GMP; DIZOCILPINE; GLYCERYL TRINITRATE; GT 1061; GUANYLATE CYCLASE; INDUCIBLE NITRIC OXIDE SYNTHASE; KETAMINE; MOLSIDOMINE; N ACETYL S NITROSOPENICILLAMINE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRIC OXIDE DONOR; NITRIC OXIDE SYNTHASE; NITROPRUSSIDE SODIUM; PHENCYCLIDINE; PLACEBO; UNCLASSIFIED DRUG;

COGNITIVE DEFECT; DOPAMINERGIC ACTIVITY; DRUG RECEPTOR BINDING; DRUG SYNTHESIS; ENZYME ACTIVATION; EXECUTIVE FUNCTION; LONG TERM MEMORY; MEMORY DISORDER; MORBIDITY; MORRIS WATER MAZE TEST; NERVE CELL PLASTICITY; NEUROPROTECTION; NEUROTOXICITY; NITRERGIC NERVE CELL; NITROSYLATION; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; OPEN FIELD TEST; PREPULSE INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; REVIEW; SCHIZOPHRENIA; ANIMAL; HUMAN; METABOLISM;

ANIMALS; HUMANS; NITRIC OXIDE; NITRIC OXIDE DONORS; SCHIZOPHRENIA;

EID: 84945951037     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2015.09.045     Document Type: Review

References (73)

1. S. Akbarian, W.E. Bunney, S.G. Potkin, S.B. Wigal, J.O. Hagman, C.A. Sandman, and E.G. Jones Altered distribution of nicotinamide-adenine dinucleotide phosphate-diaphorase cells in frontal lobe of schizophrenics implies disturbances of cortical development Arch. Gen. Psychiatry 50 1993 169 177
2. W.P. Arnold, C.K. Mittal, S. Katsuki, and F. Murad Nitric oxide activates guanylate cyclase and increases guanosine 3′5′-cyclic monophosphate levels in various tissue preparations Proc. Natl. Acad. Sci. USA 74 1977 3203 3207
3. N.S. Bamford, S. Robinson, R.D. Palmiter, J.A. Joyce, C. Moore, and C.K. Meshul Dopamine modulates release from corticostriatal terminals J. Neurosci. 24 2004 9541 9552
4. F.M. Benes, and S. Berretta GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder Neuropsychopharmacology 25 2001 1 27
5. R.J. Beninger, J.K. Forsyth, M. Van Adel, J.N. Reynolds, R.J. Boegman, and K. Jhamandas Subchronic MK-801 behavioural deficits in rats: partial reversal by the novel nitrate GT 1061 Pharmacol. Biochem. Behav. 91 2009 495 502
6. H.G. Bernstein, A. Stanarius, B. Baumann, H. Henning, D. Krell, P. Danos, P. Falkai, and B. Bogerts Nitric oxide synthase-containing neurons in the human hypothalamus: reduced number of immunoreactive cells in the paraventricular nycleus of depressed patients and schizophrenics Neuroscience 83 1998 867 875
7. H.G. Bernstein, G. Keilhoff, J. Steiner, H. Dobrowolny, and B. Bogerts Nitric oxide and schizophrenia: present knowledge and emerging concepts of therapy CNS Neurol. Disord. Drug Targets 10 2011 792 807
8. B.K. Bitanihirwe, and T.U. Woo Oxidative stress in schizophrenia: an integrated approach Neurosci. Biobehav. Rev. 35 2011 878 893
9. D.S. Bredt, and S.H. Snyder Nitric oxide, a novel neuronal messenger Neuron 8 1989 3 11
10. D.S. Bredt Endogenous nitric oxide synthesis: biological functions and pathophysiology Free Radic Res. 31 1999 577 596
11. J.E. Brenman, and D.S. Bredt Synaptic signaling by nitric oxide Curr. Opin. Neurobiol. 7 1997 374 378
12. M. Bujas-Bobanovic, D.C. Bird, H.A. Robertson, and S.M. Dursun Blockade of phencyclidine-induced effects by a nitric oxide donor Br. J. Pharmacol. 130 2000 1005 1012
13. V. Calabrese, C. Mancuso, M. Calvani, E. Rizzitelli, D.A. Butterfield, and A.M. Stella Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity Nat. Rev. Neurosci. 8 2007 766 775
14. V. Calabrese, E. Guagliano, M. Sapienza, M. Panebianco, S. Calafato, E. Puleo, G. Pennisi, C. Mancuso, D.A. Butterfield, and A.G. Stella Redox regulation of cellular stress response in aging and neurodegenerative disorders: role of vitagenes Neurochem. Res. 32 2007 757 773
15. C.M. Connor, Y. Guo, and S. Akbarian Cingulate white matter neurons in schizophrenia and bipolar disorder Biol. Psychiatry 66 2009 486 493
16. A. Contestabile, B. Monti, A. Contestabile, and E. Ciani Brain nitric oxide and its dual effect in neuroprotection/neurodegeneration: understanding molecular mechanisms to devise drug approaches Curr. Med. Chem. 10 2003 1241 1253
17. I. Das, N.S. Khan, B.K. Puri, and S.R. Hirsch Elevated endogenous nitric oxide synthase inhibitor in schizophrenic plasma may reflect abnormalities in brain nitric oxide production Neurosci. Lett. 215 1996 209 211
18. I. Das, C.N. Ramchand, A. Gliddon, and S.R. Hirsch Nitric oxide, free radicals and polyamines may have a role in membrane pathology of schizophrenia Neuropsychobiology 37 1998 65 67
19. V.L. Dawson, T.M. Dawson, E.D. London, D.S. Bredt, and S.H. Snyder Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures Proc. Natl. Acad. Sci. USA 88 1991 6368 6371
20. M.N.M. De Lima, J. Presti-Torres, A. Dornelles, S.F. Scalco, R. Roesler, V.A. Garcia, and N. Schroeder Modulatory influence of dopamine receptors on consolidation of object recognition memory Neurobiol. Learn. Mem. 95 2011 305 310
21. L. de Oliveira, C.M. Spiazzi, T. Bortolin, L. Canever, F. Petronilho, F.G. Mina, F. Dal-Pizzol, J. Quevedo, and A.I. Zugno Different sub-anesthetic doses of ketamine increase oxidative stress in the brain of rats Prog. Neuropsychopharmacol. Biol. Psychiatry 33 2009 1003 1008
22. S.L. Eastwood, and P.J. Harrison Interstitial white matter neurons express less reelin and are abnormally distributed in schizophrenia: towards an integration of molecular and morphologic aspects of the neurodevelopmental hypothesis Mol. Psychiatry 8 2003 821 831
23. T.M. Edwards, and N.S. Rickard New perspectives on the mechanisms through which nitric oxide may affect learning and memory processes Neurosci. Biobehav. Rev. 31 2007 413 425
24. J.R. Field, A.G. Walker, and P.J. Conn Targeting glutamate synapses in schizophrenia Trends Mol. Med. 17 2011 689 698
25. R. Freedman Schizophrenia N Engl. J. Med. 349 2003 1738 1749
26. R.F. Furchgott, and J.V. Zawadzki The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine Nature 288 1980 373 376
27. L.S. Garcia, C.M. Comim, S.S. Valvassori, G.Z. Reuz, L. Sterz, F. Kapczinski, E.C. Gavioli, and J. Quevedo Ketamine treatment reverses behavioral and physiological alterations induced by chronic mild stress in rats Prog. Neuropsychopharmacol. Biol. Psychiatry 33 2009 450 455
28. J. Garthwaite, S.L. Charles, and R. Chess-Williams Endothelium-derived relaxing factor release on activation of NMDA receptors suggests a role as intercellular messenger in the brain Nature 336 1988 385 387
29. J. Garthwaite Concepts of neural nitric oxide-mediated transmission Eur. J. Neurosci. 27 2008 2783 2802
30. M. Godinez-Rubi, A.E. Rojas-Mayorquin, and D. Ortuno-Sahagun Nitric oxide donors as neuroprotctive agents after an ischemic stroke-related inflammatory reaction Oxid. Med. Cell. Longev. 2013 1 16
31. I. Gourgiotis, N. Kampouri, V. Koulouri, I. Lempesis, M. Prasinou, G. Georgiadou, and N. Pitsikas Nitric oxide modulates apomorphine-induced recognition memory deficits in rats Pharmacol. Biochem. Behav. 102 2012 507 514
32. J.E.C. Hallak, J.P. Maia-de-Oliveira, J. Abrao, P.R. Evora, A.W. Zuardi, J.A.S. Crippa, P. Belmonte-de-Abreu, G.B. Baker, and S.M. Dursun Rapid improvement of acute schizophrenia symptoms after intravenous sodium nitroprusside: a randomized, double-blind, placebo-controlled trial JAMA Psychiatry 70 2013 668 676
33. J.B. Hibbs Jr., R.R. Taintor, Z. Vavrin, and E.M. Rachlin Nitric oxide: a cytotoxic activated macrophage effector molecule Biochem. Biophys. Res. Commun. 157 1988 87 94
34. K.E. Hoque, R.P. Indorkar, S. Sammut, and A.R. West Impact of dopamine-glutamate interactions on striatal neuronal nitric oxide synthase activity Psychopharmacology 207 2010 571 581
35. A.C. Issy, J.F.C. Pedrazzi, B.H. Yoneyama, and E.A. Del Bel Critical role of nitric oxide in the modulation of prepulse inhibition in Swisss mice Psychopharmacology 231 2014 663 672
36. D.C. Javitt Glutamate and schizophrenia: phencyclidine, N-methyl-d-aspartate receptors, and dopamine-glutamate interactions Int. Rev. Neurobiol. 78 2007 69 108
37. L. Kandratavicius, P.A. Balista, D.C. Wolf, J. Abrao, P.R. Evora, A.J. Rodriguez, C. Chaves, J.P. Maia-de-Oliveira, J.P. Leite, S.M. Dursun, B.G. Baker, F.S. Guimaraes, and J.E.C. Hallak Effects of the nitric oxide-related compounds in the acute ketamine animal model of schizophrenia BMC Neurosci. 16 2015 9
38. G. Keilhoff, A. Becker, G. Grecksch, G. Wolf, and H.G. Bernstein Repeated application of ketamine to rats induces changes in the hippocampal expression of parvalbumin, neuronal nitric oxide synthase and cFOS expression similar to those found in human schizophrenia Neuroscience 126 2004 591 598
39. L. Kirchner, R. Weitzdorfer, H. Hoeger, A. Uri, P. Schmidt, M. Engelmann, S.R. Villar, M. Fountoulakis, G. Lubec, and B. Lubec Impaired cognitive performances in neuronal nitric oxide synthase knockout mice is associated with hippocampal protein derangements Nitric Oxide 11 2004 316 330
40. T. Kleppisch Phosphodiesterases in the central nervous system Handb. Exp. Pharmacol. 191 2009 71 92
41. R.G. Knowles, and S. Moncada Nitric oxide synthases in mammals Biochem. J. 298 1994 249 258
42. M. Lauer, S. Johannes, S. Fritzen, D. Senitz, P. Riederer, and A. Reif Morphological abnormalities in nitric-oxide-synthase-positive striatal interneurons of schizophrenic patients Neuropsychobiology 52 2005 111 117
43. B.H. Lee, and Y.K. Kim Reduced plasma nitric oxide metabolites before and after antipsychotic treatment in patients with schizophrenia compared to controls Schizophr. Res. 104 2008 36 43
44. D. Lewis, J. Pierri, D. Volk, D. Melchitzky, and T. Woo Altered GABA neurotransmission and prefrontal cortical dysfunction in schizophrenia Biol. Psychiatry 46 1999 616 626
45. D.S. Lorrain, and E.M. Hull Nitric oxide increases dopamine and serotonin release in the medial preoptic area Neuroreport 5 1993 87 89
46. J.P. Maja-de-Oliveira, B. Lobao-Soares, T. Ramalho, E.C. Gavioli, V.P. Soares, L. Teixeira, G.B. Baker, M.S. Dursun, and J.E.C. Hallak Nitroprusside single-dose prevents the psychosis-like behavior induced by ketamine in rats up to one week Schizophr. Res. 162 2015 211 215
47. J.P. Maja-de-Oliveira, J. Abrao, P.R. Evora, A.W. Zuardi, J.A.S. Crippa, P. Belmonte-de-Abreu, G.B. Baker, M.S. Dursun, and J.E.C. Hallak The effects of sodium nitroprusside on cognitive deficits in schizophrenia: a pilot study J. Clin. Psychopharmacol. 35 2015 83 85
48. S. Mariotto, L. Cuzzolin, A. Adami, P. Del Soldato, A. Suzuki, and G. Benoni Inhibition by sodium nitroprusside of the expression of inducible nitric oxide synthase in rat neutrophils Br. J. Pharmacol. 114 1995 1105 1106
49. M.J. Menconi, N.N. Unno, M. Smith, D.E. Aguirre, and M.P. Fink Nitric oxide donor induced hyperpermeability of cultured intestinal epithelial monolayers: role of superoxide radical, hydroxyl radical, and peroxynitrite Biochim. Biophys. Acta 1425 1998 189 203
50. J. Merrill, L.J. Ignarro, M.P. Sherman, J. Melinek, and T.E. Lane Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide J. Immunol. 151 1993 2132 2141
51. M.R. Miller, and I.L. Megson Recent development in nitric oxide donor drugs Br. J. Pharmacol. 151 2007 305 321
52. U. Muller Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honey-bees Neuron 27 2000 159 168
53. Y. Nakano, R. Yoshimura, H. Nakano, A. Ikenouchi-Sugita, H. Hori, W. Umene-Nakano, N. Ueda, and J. Nakamura Association between plasma nitric oxide metabolites levels and negative symptoms of schizophrenia: a pilot study Hum. Psychopharmacol. 25 2010 139 144
54. R.M.J. Palmer, A.G. Ferrige, and S. Moncada Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor Nature 327 1987 524 526
55. N. Pitsikas, S. Zisopoulou, and N. Sakellaridis Nitric oxide donor molsidomine attenuates psychotomimetic effects of the NMDA receptor antagonist MK-801 J. Neurosci. Res. 84 2006 299 305
56. H. Prast, and A. Philippu Nitric oxide as modulator of neuronal function Prog. Neurobiol. 64 2001 51 68
57. J. Pratt, C. Winchester, N. Dawson, and B. Morris Advancing schizophrenia drug discovery: optimizing rodent models to bridge the translational gap Nat. Rev. Drug Discov. 11 2012 560 579
58. J. Ramirez, R. Garnica, M.C. Boll, S. Montes, and C. Rios Low concentrations of nitrite and nitrate in the cerebrospinal fluid from schizophrenic patients Schizophr. Res. 68 2004 357 361
59. A. Reif, S. Herterich, A. Strobel, A.C. Ehlis, D. Saur, C.P. Jacob, T. Wienker, T. Topner, S. Fritzen, U. Walter, A. Schmitt, A.J. Fallgatter, and K.P. Lesch A neuronal nitric oxide (NOS-1) haplotype associated with schizophrenia modifies prefrontal cortex function Mol. Psychiatry 11 2006 286 300
60. M. Robello, C. Amico, G. Bucossi, A. Cupello, M.V. Rapallino, and S. Thellung Nitric oxide and GABAA receptor function in the rat cerebral cortex and cerebellar granule cells Neuroscience 74 1996 99 105
61. M.G. Salgo, E. Bermudez, G.L. Squadrito, and W.A. Pryor Peroxynitrite causes DNA damage and oxidation of thiols in rat thymocytes Arch. Biochem. Biophys. 322 1995 500 505
62. S. Sammut, K.E. Bray, and A.R. West Dopamine D2 receptor-dependent modulation of striatal NO synthesis activity Psychopharmacology 191 2007 793 803
63. R. Scatena, P. Bottoni, A. Pontoglio, and B. Giardina Pharmacological modulation of nitric oxide release: new pharmacological perspectives, potential benefits and risks Curr. Med. Chem. 17 2010 61 73
64. H. Steeds, R.L. Carhart-Harris, and J.M. Stone Drug models of schizophrenia Ther. Adv. Psychopharmacol. 5 2015 43 58
65. J.R. Steinert, T. Chernova, and I.D. Forsythe Nitric oxide signaling in brain function, dysfunction and dementia Neuroscientist 16 2010 435 452
66. A.J. Susswein, A. Katzoff, N. Miller, and I. Hurwitz Nitric oxide and memory Neuroscientist 10 2004 153 162
67. E. Suzuki, T. Nakaki, M. Nakamura, and H. Miyaoka Plasma nitrite levels in deficit versus non-deficit forms of schizophrenia J. Psychiatry Neurosci. 28 2003 288 292
68. H. Wang, and V.M. Pickel Dopamine D2 receptors are present in the prefrontal cortical afferents and their targets in patches of the rat caudate-putamen nucleus J. Comp. Neurol. 442 2002 392 404
69. A.R. West, M.P. Galloway, and A.A. Grace Regulation of striatal dopamine neurotransmission by nitric oxide: effector pathways and signalling mechanisms Synapse 44 2002 227 245
70. J.L. Wiley, K.M. Golden, and S.E. Bowen Effects of modulation of nitric oxide on acoustic startle responding and prepulse inhibition in rats Eur. J. Pharmacol. 328 1997 125 130
71. G. Xing, M. Chavko, L.X. Zhang, S. Yang, and R.M. Post Decreased calcium-dependent constitutive nitric oxide synthase (eNOS) activity in prefrontal cortex in schizophrenia and depression Schizophr. Res. 58 2002 21 30
72. 2 receptor-operated protein phosphatase gate J. Neurosci. 29 2009 14086 14099
73. K. Yamada, Y. Noda, T. Hasegawa, Y. Komori, T. Nikai, H. Sugihara, and T. Nabeshima The role of nitric oxide in dizocilpine-induced impairment of spontaneous alternation behavior in mice J. Pharmacol. Exp. Ther. 276 1996 460 466