Role of nitric oxide in patients with schizophrenia - A systematic review of the literature

Current Psychiatry Reviews

Volumn 4, Issue 4, 2008, Pages 219-227

  Oliveira, Joao Paulo ^a   Zuardi, Antonio Waldo ^a   Hallak, Jaime Eduardo ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Nitric oxide; Schizophrenia

Indexed keywords

CHROMOSOME PROTEIN; CLOZAPINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROLEPTIC AGENT; NEURONAL NITRIC OXIDE SYNTHASE; NEUROPEPTIDE; NEUROTRANSMITTER; NITRIC OXIDE; OLANZAPINE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RISPERIDONE;

BASAL GANGLION; BIOCHEMISTRY; CEREBELLUM; ENVIRONMENTAL FACTOR; HEREDITY; HISTOCHEMISTRY; HUMAN; HYPOTHALAMUS; LEARNING; MEMORY; NERVE CELL DIFFERENTIATION; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; PREFRONTAL CORTEX; PRIORITY JOURNAL; REVIEW; SCHIZOPHRENIA; SYSTEMATIC REVIEW; TEMPORAL CORTEX;

EID: 65949112716     PISSN: 15734005     EISSN: None     Source Type: Journal    
DOI: 10.2174/157340008786576553     Document Type: Review

References (93)

1. Meltzer HY, Stahl SM. The dopamine hypothesis of schizophrenia: a review. Schizophr. Bull 1976; 2: 19-76.
2. Seeman P, Lee T, Chau-Wong M, Wong K. Antipsychotic drug doses and neuroleptic/dopamine receptors. Nature 1976; 261: 717-719.
3. Reynolds GP. Increased concentrations and lateral asymmetry of amygdala dopamine in schizophrenia. Nature 1983; 305: 527-529.
4. Johnstone E, Crow TJ, Frith CD, Carvey MW, Price JS. Mechanism of the antipsychotic effect in treatment of chronic schizophrenia. Lancet 1978; 1: 848-851.
5. Reynolds GP. Beyond the dopamine hypothesis. Tile neurochemical pathology of schizophrenia. Br J Psychiatry 1989; 155: 305-316.
6. Sulzer D, Rayport S. Amphetamine and other psychostimulants reduce pH gradients in midbrain dopamine neurons and chromaffin granules: a mechanism of action. Neuron 1990; 5: 797-808.
7. Sulzer D, Chen TK, Lau YY, Kristensen H, Rayport S, Ewing A. Amphetamine redistributes dopamine from synaptic vesicles to the cytosol and promotes reverse transport. J Neurosci 1995; 15: 4102-4108.
8. Liang NY, Rutledge CO. Evidence for carrier-mediated efflux of dopamine from corpus striatum. Biochem. Pharmacol 1982; 31: 2479-2484.
9. Kahlig KM, Binda F, Khoshbouei H, et al. Amphetamine induces dopamine efflux through a dopamine transporter channel. Proc Natl Acad Sci USA 2005; 102: 3495-3500.
10. Bell DS. Comparison of amphetamine psychosis and schizophrenia. Br. J. Psychiatry 1965; 111: 701-707.
11. Kramer JC, Fischman VS, Littlefield DC. Amphetamine abuse. Pattern and effects of high doses taken intravenously. J Am Med Assoc 1967; 201 (5): 305-309.
12. Snyder SH. Amphetamine psychosis: a 'model' schizophrenia mediated by catecholamines. Am J Psychiatry 1973; 130 (1): 61-67.
13. Lipska BK, Jaskiw GE, Weinberger DR. Postpubertal emergence of hyperresponsiveness to stress and to amphetamine after neonatal excitotoxic hippocampal damage: a potential model of schizophrenia. Neuropsychopharmacology 1993; 9: 67-75.
14. Luby ED, Cohen BD, Rosenbaum G, Gottlieb JS, Kelley R. Study of a new schizophrenomimetic drug-Sernyl. Am Med Assoc Arch Neurol Psychiatry 1959; 81: 363-369.
15. Siegel RK. Phencyclidine and ketamine intoxication: a study of four populations of recreational users. NIDA Res Monogr 1978; 21: 119-147.
16. Toru M, Kuramaji A, Ishimaru M. Excitatory amino acids: implications for psychiatric disorders research. Life Sci 1994; 55: 1683-1699.
17. Steinpreis RE. The behavioural and neurochemical effects of phencyclidine in humans and animals: some implications for modelling psychosis. Behav Brain Res 1996; 74: 45-55.
18. Jentsch JD, Redmond DE, Elsworth JD, Taylor JR, Youngren KD, Roth RH. Enduring cognitive deficits and cortical dopamine dysfunction in monkeys after long-term administration of phencyclidine. Science 1997; 277: 953-955.
19. Garthwaite J. Glutamate, nitric oxide and cell - cell signaling in the nervous system. Trends Neurosci 1991; 14 (2): 60-67.
20. Dawson TM, Snyder SH. Gases as biological messengers: nitric oxide and carbon monoxide in the brain. J Neurosci 1994; 14: 5147-5159.
21. Osawa Y, Davila JC. Phencyclidine, a psychotomimetic agent and drug of abuse, is a suicide inhibitor of brain nitric oxide synthase. Biochem Biophys Res Comm 1993; 194: 1435-1439.
22. Chetty CS, Hussain S, Slikker W, Ali SF. Effects of phencyclidine on nitric oxide synthase activity in different regions of rat brain. Res Comm Alco Subst Abuse 1995; 16: 105-114.
23. Noda Y, Yamada K, Komori Y, Sugihara H, Furukawa H, Nabeshima T. Role of nitric oxide in the development of tolerance and sensitization to behavioural effects of phencyclidine in mice. Br J Pharmacol 1996; 117: 1579-1585.
24. Bredt DS, Snyder SH. Nitric oxide, a novel neuronal messenger. Neuron 1992; 8: 3-11.
25. Bhagat K, Vallance P. Nitric oxide 9 years on. J R Soc Med 1996; 89 (12): 667-673.
26. Segovia G, Mora F. Role of the nitric oxide in modulating the release of dopamine, glutamate, and GABA in striatum of the freely moving rat. Brain Res Bull 1998; 45: 275-279.
27. Ignarro LJ. Haem-dependent activation of guanylate cyclase and cyclic GMP formation by endogenous nitric oxide: a unique transduction mechanism for transcellular signaling. Pharmacol Toxicol 1990; 67: 1-7.
28. Ignarro LJ, Murad F. Nitric oxide: Biochemistry, Molecular Biology and Therapeutic Implications. San Diego: Academic Press, 1995.
29. McDonald LJ, Murad F. Nitric oxide and cyclic GMP signaling. Proc Soc Exp Biol Med 1996; 211: 1-6.
30. Russwurm M, Koesling D. Guanyl cyclase: NO hits its target. Biochem Soc Symp 2004; 71: 51-63.
31. Mayer B, Schmidt K, Humbert P, Bohme E. Biosynthesis of endothelium-derived relaxing factor: a cytosolic enzyme in porcine aortic endothelial cells Ca2-dependently converts Larginine into an activator of soluble guanylyl cyclase. Biochem Biophys Res Comm 1989; 164 (2): 678-685, 660-669.
32. Dawson TM, Snyder SH. Gases as biological messengers: nitric oxide and carbon monoxide in the brain. J Neurosci 1994; 14: 5147-5159.
33. Lonart G, Wang J, Johnson KM. Nitric oxide induces neurotransmitter release from hippocampal slices. Eur J Pharmacol 1992; 220 (2-3): 271-272.
34. Black MD, Matthews EK, Humphrey PP. The effects of a photo-sensitive nitric oxide donor on basal and electrically stimulated dopamine efflux from the rat striatum in vitro. Neuropharmacology 1994; 33 (11): 1357-1365.
35. Holscher C. Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity. Trends Neurosci 1997; 20 (7): 298-303.
36. Gally JA, Montague PR, Reeke GNJr, Edelman GM. The NO hypothesis: possible effects of a short-lived, rapidly diffusible signal in the development and function of the nervous system. Proc Natl Acad Sci 1990; 87 (9): 3547-3551.
37. Hess DT, Patterson SI, Smith DS, Skene JH. Neuronal growth cone collapse and inhibition of protein fatty acylation by nitric oxide. Nature 1993; 366: 562-565.
38. Ogilvie P, Schilling K, Billingsley ML, Schmidt HH. Induction and variants of neuronal nitric oxide synthase type I durin synaptogenesis. FASEB J 1995; 9 (9): 799-806.
39. Wu HH, Waid DK, McLoon SC. Nitric oxide and the developmental remodeling of retinal connections in the brain. Prog Brain Res 1996; 108: 273-286.
40. Bravo H, Inzunza O, Fernandez V, Sanhueza M. Distribution of NADPH-d positive neurons during postnatal development of the rat somatosensory cortex correlates with gradients of neurogenesis and development. Neurosci Lett 1997; 234 (2-3): 103-106.
41. Hindley S, Juurlink BH, Gysbers JW, Middlemiss PJ, Herman MA, Rathbone MP. Nitric oxide donors enhance neurotrophin-induced neurite outgrowth through a cGMP-dependent mechanism. J Neurosci Res 1997; 47 (4): 427-439.
42. Das I, Khan NS, Puri BK, Sooranna SR, de Belleroche J, Hirsch SR. Elevated platelet calcium mobilizationand nitric oxide synthase activity may reflect abnormalities in schizophrenic brain. Biochem Biophys Res Commun 1995; 212: 375-380.
43. Akyol O, Herken H, Uz E, et al. The indices of endogenous oxidative and antioxidative processes in plasma from schizophrenic patients. The possible role of oxidant/antioxidant imbalance. Prog Neuropsychopharmacol Biol Psychiatry 2002; 26(5): 995-1005.
44. Li HC, Chen QZ, Ma Y, Zhou JF. Imbalanced free radicals and antioxidant defense systems in schizophrenia: a comparative study. J Zhejiang Univ Sci B 2006; 7(12): 981-6.
45. Herken H, Uz E, Ozyurt H, Akyol O. Red blood cell nitric oxide levels in patients with schizophrenia. Schizophr Res 2001; 52(3): 289-90.
46. Zoroglu SS, Herken H, Yurekli M, et al. The possible pathophysiological role of plasma nitric oxide and adrenomedullin in schizophrenia. J Psychiatr Res 2002; 36: 309-315.
47. Yilmaz N, Herken H, Cicek A, Celik A, Yurekli M, Akyol O. Increased levels of nitric oxide, cortisol and adrenomedullin in patients with chronic schizophrenia. Med Princ Pract 2006; 16(2): 137-41.
48. Richards AM, Nichoils MG, Lewis L, Lainch-bury JG. Adrenomedullin. Clinical Science 1996; 91: 3-16.
49. Wink DA, Hanbauer I, Krishna MC, De Graff W, Gamson J, Mitchell JB. Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species. Proc Nat Acad Sci USA 1993; 90: 9813-7.
50. Das I, Khan NS, Puri BK, Hirsch SR. Elevated endogenous nitric oxide synthase inhibitor in schizophrenic plasma may reflect abnormalities in brain nitric oxide production. Neurosci Lett 1996; 215(3): 209-11.
51. Srivastava N, Barthwal MK, Dalal PK, et al. Nitrite content and antioxidant enzyme levels in the blood of schizophrenic patients. Psychopharmacology 2001; 158: 140-145.
52. Yanik M, Vural H, Tutkun H, et al. Is the arginine-nitric oxide pathway involved in the pathogenesis of schizophrenia? Neuropsychobiology 2003; 47: 61-65.
53. Suzuki E, Nakaki T, Nakamura M, Miyaoka H. Plasma nitrate levels in deficit versus non-deficit forms of schizophrenia. J Psychiatr Neurosci 2003; 28: 288-292.
54. Ramirez J, Garnica R, Boll MC, Montes S, Rios C. Low concentration of nitrite and nitrate in the cerebrospinal fluid from schizophrenic patients: a pilot study. Schizophr Res 2004; 68(2-3): 357-61.
55. Richardson MA, Read LL, Clelland CL, et al. Evidence for a tetrahydrobiopterin deficit in schizophrenia. Neuropsychobiology 2005; 52: 190-201.
56. Fiege B, Ballhausen D, Kierat L, et al. Plasma tetrahydrobiopterin and its pharmacokinetic following oral administration. Mol Genet Metab 2004; 81: 45-51.
57. Kaufman S. Tetrahydrobiopterin. Basic biochemistry and role in human disease. Jonhs Hopkins University Press, Baltimore 1997.
58. Barker JE, Strangward HM, Brand MP, et al. Increased inducible nitric oxide synthase protein but limited nitric oxide formation occurs in astrocytes of the hph-1(tetrahydrobiopterin deficient) mouse. Brain Res 1998; 804: 1-6.
59. Richardson MA, Read LL, Reilly MA, Clelland CLAnalysis of plasma biopterin levels in psychiatric disorders suggests a common BH4 deficit in schizophrenia and schizoaffective disorder. Neurochem Res 2007; 32(1): 107-13.
60. Yao JK, Leonard S, Reddy RD. Increased nitric oxide radicals in postmortem brain from patients with schizophrenia. Schizophr. Bull 2004; 30(4): 923-34.
61. Lauer M, Johannes S, Fritzen S, Senitz D, Riederer P, Reif A. Morphological abnormalities in nitric-oxide-synthase-positive striatal interneurons of schizophrenic patients. Neuropsychobiology 2005; 52(3): 111-7.
62. Fritzen S, Lauer M, Schmitt A, et al. NO synthase-positive striatal interneurons are decreased in schizophrenia. Eur Neuropsychopharmacol 2007; 17: 595-599
63. Doyle CA, Slater P. Application of [3H] L-NG-nitroarginine labelling to measure cerebellar nitric oxide synthase in patients with schizophrenia. Neurosci Lett 1995; 202: 49-52.
64. Karson CN, Griffin WST, Mrak RE, et al. Nitric oxide synthase (NOS) in schizophrenia: increases in cerebellar vermis. Mol Chem Neuropathol 1996; 27(3): 275-84.
65. Bernstein HG, Krell D, Braunewell KH, et al. Increased number of nitric oxide synthase immunoreactive Purkinje cells and dentate nucleus neurons in schizophrenia. J Neurocytol 2001; 30(8): 661-70.
66. Bernstein HG, Stanarius A, Baumann B, et al. Nitric oxide synthase-containing neurons in the human hypothalamus: reduced number of immunoreactive cells in the paraventricular nucleus of depressive patients and schizophrenics. Neuroscience 1998; 83(3): 867-75.
67. Bernstein HG, Jirikowski GF, Heinemann A, et al. Low and infrequent expression of nitric oxide synthase/NADPH-diaphorase in neurons of the human supraoptic nucleus: a histochemical study. J Chem Neuroanat 2000; 20(2): 177-83.
68. Xing G, Chavko M, Zhang LX, Yang S, Post RM. 2002. Decreased calcium-dependent constitutive nitric oxide synthase (cNOS) activity in prefrontal cortex in schizophrenia and depression. Schizophr Res 2002; 58: 21-30.
69. Xu B, Wratten N, Charych EI, Buyske S, Firestein BL, Brzustowicz LM. 2005. Increased expression in dorsolateral prefrontal cortex of CAPON in schizophrenia and bipolar disorder. PLoS Med 2005; 2 (10), e263.
70. Baba H, Suzuki T, Arai H, Emson PC. Expression of nNOS and soluble guanylate cyclase in schizophrenic brain. Neuroreport 2004; 15(4): 677-80.
71. Akbarian S, Bunney Jr. WE, Potkin SG, et al. Altered distribution of nictotin-adenine dinucleotide phosphate-diaphorase cells in frontal lobe of schizophrenics implies disturbances of cortical development. Arch Gen Psychiatry 1993a; 50: 169-177.
72. Akbarian S, Vinuela A, Kim JJ, Potkin SG, Bunney Jr. WE, Jones EG. Distorted distribution of nicotinamide adenine dinucleotide-phosphate diaphorase neurons in temporal lobe of schizophrenica implies anomalous cortical development. Arch Gen Psychiatry 1993b; 50: 78-187.
73. Akbarian S, Kim JJ, Potkin SG, Hetrick WP, Bunney Jr. WE, Jones EG. Maldistribution of interstitial neurons in prefrontal white matter of the brains of schizophrenic patients. Arch Gen Psychiatry 1996; 53: 425-436.
74. Shinkai T, Ohmori O, Hori H, Nakamura J. Allelic association of the neuronal nitric oxide synthase (NOS1) gene with schizophrenia. Mol Psychiatry 2002; 7: 560-563.
75. Fallin MD, Lasseter VK, Avramopoulos D, et al. Bipolar I disorder and schizophrenia: a 440-single-nucleotide polymorphism screen of 64 candidate genes among Ashkenazi Jewish case-parent trios. Am J Human Genetics 2005; 77: 918-936.
76. Reif A, Herterich S, Strobel A, et al. A neuronal nitric oxide synthase (NOS-I) haplotype associated with schizophrenia modifies prefrontal cortex function. Mol Psychiatry 2006; 11(3): 286-300.
77. Tang W, Huang K, Tang R, et al. Evidence for association between the 5′ flank of the NOS1 gene and schizophrenia in the Chinese population. Int J Neuropsychopharmacol 2008; 11: 1-9.
78. Liou YJ, Tsai SJ, Hong CJ, Liao DL. Association analysis for the CA repeat polymorphism of the neuronal nitric oxide synthase (NOS1) gene and schizophrenia. Schizophr Res 2003; 65(1): 57-9.
79. Brzustowicz LM, Siomne J, Mohseni P, et al. Linkage disequilibrium mapping of schizophrenia susceptibility to the CAPON region of chromosome 1q22. Am J Hum Genet 2004; 74(5): 1057-63.
80. Zheng Y, Li H, Quin W, et al. Association of the carboxy-I-terminal PDZ ligand of the neuronal nitric oxide synthase gene with schizophrenia in the Chinese Han population. Biochem Biophys Res Commun 2005; 328: 809-815.
81. Miranda A, García J, López C, et al. Putative association of the carboxy-terminal PDZ ligand of neuronal nitric oxide synthase gene (CAPON) with schizophrenia in a Colombian population. Schizophr Res 2006; 82(2-3): 283-5.
82. Puri V, McQuillin A, Thirumalai S, et al. Failure to confirm allelic association between markers at the CAPON gene locus and schizophrenia in a British sample. Biol Psychiatry 2006; 59(2): 195-7.
83. Deutsch SI, Rosse RB, Schwartz BL, Fay-McCarthy M, Rosenberg P, Fearing K. Methylene blue adjuvant therapy of schizophrenia. Clin Neuropharmacol 1997; 20(4): 357-63.
84. Taneli F, Piridar S, Akdeniz F, Uyanik BS, Ari Z. Serum nitric oxide metabolite levels and the effect of antipsychotic therapy in schizophrenia. Arch Med Res 2004; 35: 401-405.
85. Atmaca M, Tezcan E, Ustundag B. Plasma nitric oxide and leptin values in patients with olanzapine-induced weight gain. J Psychiatr Res 2007; 41(1-2): 74-9.
86. Lee BH, Kim YK. Reduced plasma nitric oxide metabolites before and after antipsychotic treatment in patients with schizophrenia compared to controls. Schizophr. Res., In press.
87. Ebstein RP, Biederman J, Rimon R, Zohar J, Belmaker RJ. Cyclic GMP in the CSF of patients with schizophrenia before and after neuroleptic treatment. Psychopharmacology 1976; 51: 71-4.
88. Smith CC, Tallman JF, Post RM. An examination of baseline and drug induced levels of cyclic nucleotides in the cerebrospinal fluid of controls and psychiatric patients. Life Sci 1976; 19: 131-6.
89. Gattaz WF, Carmer H, Beckmann H. Low CSF concentrations of cyclic GMP in schizophrenia. Br J Psychiatry 1983; 142: 288-291.
90. Ziimmer R, Teelken AW, Cramer H, Ackenheil M, Zandler KJ, Fischer H. Short- and long-term effects on GABA and dopamine neurons during treatment with sulpiride. Adv Biochem Psychopharmacol 1980; 24: 537-9.
91. Thornberg SA, Saklad SR. A review of NMDA receptors and the phencyclidine model of schizophrenia. Pharmacotherapy 1996; 16: 82-93.
92. Deakin JF, Simpson MD. A two-process theory of schizophrenia: evidence from studies in post-mortem brain. J Psychiatr Res 1997; 31: 277-95.
93. Bernstein HG, Bogerts B, Keilhoff G. The many faces of nitric oxide in schizophrenia. A review. Schizophr Res 2005; 78: 69-86.