Effects of the inducible nitric oxide synthase inhibitor aminoguanidine in two different rat models of schizophrenia

Behavioural Brain Research

Volumn 309, Issue , 2016, Pages 14-21

  Lafioniatis, Anastasios ^a   Orfanidou, Martha A ^a   Papadopoulou, Evangelia S ^a   Pitsikas, Nikolaos ^a  

^a UNIVERSITY OF THESSALY   (Greece)

Author keywords

Aminoguanidine; Apomorphine; Ketamine; Nitric oxide; Schizophrenia

Indexed keywords

AMINOGUANIDINE; APOMORPHINE; INDUCIBLE NITRIC OXIDE SYNTHASE; KETAMINE; ENZYME INHIBITOR; GUANIDINE DERIVATIVE; NEUROLEPTIC AGENT; NOS2 PROTEIN, RAT;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR DISORDER; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; DRUG ANTAGONISM; DRUG EFFICACY; GLUTAMATERGIC SYNAPSE; MALE; MEMORY DISORDER; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; PRIORITY JOURNAL; PSYCHOSOCIAL WITHDRAWAL; RAT; SCHIZOPHRENIA; SOCIAL INTERACTION TEST; SOCIAL ISOLATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; PHYSIOLOGY; PSYCHOLOGY; RANDOMIZATION; RECOGNITION; SOCIAL BEHAVIOR; WISTAR RAT;

ANIMALS; ANTIPSYCHOTIC AGENTS; APOMORPHINE; ENZYME INHIBITORS; GUANIDINES; KETAMINE; MALE; NITRIC OXIDE SYNTHASE TYPE II; RANDOM ALLOCATION; RATS, WISTAR; RECOGNITION (PSYCHOLOGY); SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY; SOCIAL BEHAVIOR;

EID: 84966429072     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2016.04.043     Document Type: Article

References (81)

1. Akbarian S., Bunney W.E., Potkin S.G., Wigal S.B., Hagman J.O., Sandman C.A., Jones E.G. Altered distribution of nicotinamide-adenine dinucleotide phosphate-diaphorase cells in frontal lobe of schizophrenics implies disturbances of cortical development. Arch. Gen. Psychiatry 1993, 50:169-177.
2. Bartolini L., Casamenti F., Pepeu G. Aniracetam restores object recognition impaired by age, scopolamine and nucleus basalis lesions. Pharmacol. Biochem. Behav. 1996, 53:277-283.
3. Bergstrom H.C., Darvesh A.S., Berger S.P. Inducible oxide inhibitors block NMDA antagonist-stimulated motoric behaviors and medial prefrontal cortical glutamate efflux. Front. Pharmacol. 2015, 292.
4. Bernstein H.G., Bogerts B., Keilhoff G. The many faces of nitric oxide in schizophrenia. A review. Schizophr. Res. 2005, 78:69-86.
5. Bernstein H.G., Keilhoff G., Steiner J., Dobrowolny H., Bogerts B. Nitric oxide and schizophrenia: present knowledge and emerging concepts of therapy. CNS Neurol. Disord. Drug Targets 2011, 10:792-807.
6. Bianchi G., Landi M., Garattini S. Disposition of apomorphine in rat brain areas: relationship to stereotypy. Eur. J. Pharmacol. 1986, 131:229-236.
7. Bitanihirwe B.K., Woo T.U. Oxidative stress in schizophrenia: an integrated approach. Neurosci. Biobehav. Rev. 2011, 35:878-893.
8. Boer R., Wolf-Rudiger U., Klein T., Mirau B., Haas S., Baur I. The inhibitory potency and selectivity of arginine substrate site nitric-oxide synthase inhibitors is solely determined by their affinity toward the different isoenzymes. Mol. Pharmacol. 2000, 58:1026-1034.
9. Boultadakis A., Pitsikas N. Effects of the nitric oxide synthase inhibitor L-NAME on recognition and spatial memory deficits produced by different NMDA receptor antagonists in the rat. Neuropsychopharmacology 2010, 35:2357-2366.
10. Bredt D.S. Endogenous nitric oxide synthesis: biological functions and pathophysiology. Free Radic. Res. 1999, 31:577-596.
11. Calev A., Venables P.H., Monk A.F. Evidence for distinct verbal memory pathologies in severely and mildly disturbed schizophrenics. Schizophr. Bull. 1983, 9:247-264.
12. Cavoy A., Delacour J. Spatial but not object recognition is impaired by aging in rats. Physiol. Behav. 1993, 53:527-530.
13. Clinton S.M., Haroutunian V., Davis K.L., Meader-Woodraff J.H. Altered transcript expression of NMDA-receptor associated postsynaptic proteins in the thalamus of subjects with schizophrenia. Am. J. Psychiatry 2003, 160:1100-1109.
14. Cools R. Role of dopamine in the motivational and cognitive control of behavior. Neuroscientist 2008, 14:381-395.
15. Costa E., Davis J.M., Dong E., Grayson D.R., Guidotti A., Tremolizzo L., Veldic M. A GABAergic cortical deficit dominates sschizpphrenia pathophysiology. Crit. Rev. Neurobiol. 2004, 16:1-23.
16. Coyle J.T. The glutamatergic dysfunction hypothesis for schizophrenia. Harv. Rev. Psychiatry 1996, 3:241-253.
17. Das I., Ramchand C.N., Gliddon A., Hirsch S.R. Nitric oxide, free radicals and polyamines may have a role in membrane pathology of schizophrenia. Neuropsychobiology 1998, 37:65-67.
18. Dawson V.L., Dawson T.M., London E.D., Bredt D.S., Snyder S.H. Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:6368-6371.
19. de Oliveira L., Spiazzi C.M., Bortolin T., Canever L., Petronilho F., Mina F.G., Dal-Pizzol F., Quevedo J., Zugno A.I. Different sub-anesthetic doses of ketamine increase oxidative stress in the brain of rats. Prog. Neuropsychopharmacol. Biol. Psychiatry 2009, 33:1003-1008.
20. Diaz A., Rojas K., Espinosa B., Chavez R., Zenteno E., Limon D., Guevara J. Aminoguanidine treatment ameliorates inflammatory responses and memory impairment induced by amyloid-beta 25-35 injection in rats. Neuropeptides 2014, 48:153-159.
21. Dingman A., Lee S.Y., Derugin N., Wenland M.F., Vexler Z.S. Aminoguanidine inhibits caspase-3 and calpain activation without affecting microglial activation following neonatal transient cerebral ischemia. J. Neurochem. 2006, 96:1467-1479.
22. Edwards J., Jackson H.J., Pattison P.E. Emotion recognition via facial expression and affective prosody in schizophrenia: a methodological review. Clin. Psychol. Rev. 2002, 22:789-832.
23. Ennaceur A., Delacour J. A new one-trial test for neurobiological studies of memory in rats. 1. Behavioral data. Behav. Brain Res. 1988, 31:47-59.
24. Everitt B.J., Robbins T.W. Central cholinergic system and cognition. Annu. Rev. Psychol. 1997, 48:649-684.
25. Field J.R., Walker A.G., Conn P.J. Targeting glutamate synapses in schizophrenia. Trends Mol. Med. 2011, 17:689-698.
26. Freedman R. Schizophrenia. N. Engl. J. Med. 2003, 349:1738-1749.
27. Garthwaite J. Glutamate nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci. 1991, 14:60-67.
28. Georgiadou G., Grivas V., Tarantilis P.A., Pitsikas N. Crocins, the active constituents of Crocus sativus L., counteracted ketamine-induced behavioural deficits in rats. Psychopharmacology 2014, 231:717-726.
29. Gibbs S.E., D'Esposito M. A functional MRI study of the effects of bromocriptine, a dopamine receptor agonist, on component processes of working memory. Psychopharmacology 2005, 180:644-653.
30. Gourgiotis I., Kampouri N.G., Koulouri V., Lempesis I.G., Prasinou M.D., Georgiadou G., Pitsikas N. Nitric oxide modulates apomorphine-induced recognition memory deficits in rats. Pharmacol. Biochem. Behav. 2012, 102:507-514.
31. Haley J.E., Wilcox G.L., Chapman P.F. The role of nitric oxide in hippocampal long-term potentiation. Neuron 1992, 8:211-216.
32. Iravani M.M., Kashefi K., Mander P., Rose S., Jenner P. Involvement of inducible nitric oxide synthase in inflammation-induced dopaminergic neurodegeneration. Neuroscience 2002, 110:49-58.
33. Iversen S.D., Iversen L.L. Dopamine: 50 years in perspective. Trends Neurosci. 2007, 30:188-193.
34. Javitt D.C., Zukin S.R. Recent advances in the phencyclidine model of schizophrenia. Am. J. Psychiatry 1991, 148:1301-1308.
35. Johansson C., Jackson D.M., Svensson L. Nitric oxide synthase inhibition blocks phencyclidine-induced behavioural effects on prepulse inhibition and locomotor activity in the rat. Psychopharmacology 1997, 131:167-173.
36. Klamer D., Engel J.A., Svensson L. The nitric oxide synthase inhibitor, L-NAME, block phencyclidine-induced disruption of prepulse inhibition in mice. Psychopharmacology 2001, 156:182-186.
37. Klamer D., Engel J.A., Svensson L. The neuronal selective nitric oxide synthase inhibitor, Nomega-propyl-l-arginine, blocks the effects of phencyclidine on prepulse inhibition and locomotor activity in mice. Eur. J. Pharmacol. 2004, 503:103-107.
38. Klamer D., Palsson E., Wass C., Archer T., Engel J.A., Svensson L. Antagonism of the nitric oxide synthase inhibitor L-NAME, of the effects of phencyclidine on latent inhibition in taste aversion conditioning. Behav. Brain Res. 2005, 161:60-68.
39. Koros E., Rosenbrock H., Birk G., Weiss C., Sams-Dodd F. The selective mGlu5 receptor antagonist MTEP, similar to NMDA receptor antagonists, induces social isolation in rats. Neuropsychopharmacology 2007, 32:562-576.
40. Krystal J.H., Karper L.P., Seibyl J.P., Freeman G.K., Delaney R., Bremmer J.D., Heninger G.R., Bowers M.B., Chamey D.S. Sub-anesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans psychotomimetic, perceptual, cognitive and neuroendocrine responses. Arch. Gen. Psychiatry 1994, 51:199-214.
41. Lahti A.C., Weiler M.A., Tamara Michaelidis B.A., Parwani A., Tamminga C.A. Effects of ketamine in normal and schizophrenic volunteers. Neuropsychopharmacology 2001, 25:455-467.
42. Lynch G., Staubli V. Possible contributions of long-term potentiation to the encoding and organization of memory. Brain Res. 1991, 16:204-206.
43. Malhotra A.K., Pinals D.A., Adler C.M., Elman I., Clifton A., Pickar D., Breier A. Ketamine-induced exacerbation of psychotic symptoms and cognitive impairment in neuroleptic-free schizophrenics. Neuropsychopharmacology 1997, 17:141-150.
44. McGrath J., Saha S., Chant T., Welham J. Schizophrenia: a concise overview of incidence, prevalence, and mortality. Epidemiol. Rev. 2008, 30:67-76.
45. McNaught K.S., Jenner P. Altered glial function causes neuronal death and increases neuronal susceptibility to 1-methyl-4-phenylpyridinium- and 6-hydroxydopamine-induced toxicity in astrocytic/ventral mesencephalic co-cultures. J. Neurochem. 1999, 73:2469-2475.
46. Moghaddam B., Adams B., Verma A., Daly D. Activation of glutamatergic neurotransmission by ketamine: a novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex. J. Neurosci. 1997, 17:2921-2927.
47. Monte A.S., de Souza G.C., McIntyre R.S., Soczynska J.K., dos Santos J.V., Cordeiro R.C., Ribeiro B.M., de Lucena D.F., Vasconcelos S.M., de Souza F.C., Carvalho A.F., Macedo D.S. Prevention and reversal of ketamine-induced schizophrenia related behavior by minocycline in mice: possible involvement of antioxidant and nitrergic pathways. J. Psychopharmacol. 2013, 27:1032-1043.
48. Montoya A., Lal S., Menear M., Duplessis E., Thavundayil J., Schmitz N., Lepage M. Apomorphine effects on episodic memory in young healthy volunteers. Neuropsychologia 2008, 46:292-300.
49. Morgan C.J., Mofeez A., Brandner B., Bromley L., Curran H.V. Acute effects of ketamine on memory systems and psychotic symptoms in healthy volunteers. Neuropsychopharmacology 2004, 29:208-218.
50. Mori K., Togashi H., Ueno K.I., Matsumoto M., Yoshika M. Aminoguanidine prevented the impairment of learning behavior and hippocampal long-term potentiation following transient cerebral ischemia. Behav. Brain Res. 2001, 120:159-168.
51. Neill J.C., Barnes S., Cook S., Grayson B., Idris N.F., McLean S.L., Snigdha S., Rajagopal L., Harte M.K. Animal models of cognitive dysfunction and negative symptoms of schizophrenia: focus on NMDA receptor antagonism. Pharmacol. Ther. 2010, 128:419-432.
52. O'Dell T.J., Hawkins R.D., Kandel E.R., Arancio O. Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:11285-11289.
53. O'shea M., McGregor I.S., Mallet P.E. Repeated cannabinoid exposure during perinatal, adolescent or early adult ages produces similar long-lasting deficits in object recognition and reduced social interaction in rats. J. Psychopharmacol. 2006, 20:611-621.
54. Pitsikas N., Rigamonti A.E., Cella S.G., Muller E.E. Effects of the nitric oxide donor molsidomine on different memory components as assessed in the object recognition task in the rat. Psychopharmacology 2002, 162:239-245.
55. Pitsikas N., Boultadakis A., Sakellaridis N. Effects of sub-anesthetic doses of ketamine on rats' spatial and non-spatial recognition memory. Neuroscience 2008, 154:454-460.
56. Prast H., Philippu A. Nitric oxide as modulator of neuronal function. Prog. Neurobiol. 2001, 64:51-68.
57. Ramirez J., Garnica R., Boll M.C., Montes S., Rios C. Low concentrations of nitrite and nitrate in the cerebrospinal fluid from schizophrenic patients. Schizophr. Res. 2004, 68:357-361.
58. Reif A., Herterich S., Strobel A., Ehlis A.C., Saur D., Jacob C.P., Wienker T., Topner T., Fritzen S., Walter U., Schmitt A., Fallgatter A.J., Lesch K.P. A neuronal nitric oxide (NOS-1) haplotype associated with schizophrenia modifies prefrontal cortex function. Mol. Psychiatry 2006, 11:286-300.
59. Roberts R.C., Roche J.K., Conley R.R. Synaptic differences in the post-mortem striatum of subjects with schizophrenia: a stereological and ultrastructural analysis. Synapse 2005, 56:185-197.
60. Rodriguez L., Biasibetti R., Swarowsky A., Leite M.C., Quincozes-Santos A., Quilfeldt J.A., Achaval M., Goncalves C.A. Hippocampal alterations in rats submitted to streptozocin-induced dementia model are prevented by aminoguanidine. J. Alzheimers Dis. 2009, 17:193-202.
61. Salum C., Guimaraes F.S., Brandao M.L., Del Bel E.A. Dopamine and nitric oxide interaction on the modulation of PPI of the acoustic startle response in the Wistar rat. Psychopharmacology 2006, 185:133-141.
62. Salum C., Issy A.C., Brandao M.L., Guimaraes F.S., Del Bel E.A. Nitric oxide modulates dopaminergic regulation of prepulse inhibition in the basolateral amygdala. J. Psychopharmacol. 2011, 25:1639-1648.
63. Sams-Dodd F. Phencyclidine-induced stereotyped behaviour and social isolation in rats: a possible animal model of schizophrenia. Behav. Pharmacol. 1996, 7:3-23.
64. Seillier A., Giuffrida A. Evaluation of NMDA receptor models of schizophrenia: divergences in the behavioral effects of sub-chronic PCP and MK-801. Behav. Brain Res. 2009, 204:410-415.
65. Shibata H., Katsuki H., Nishiwaki M., Kume T., Kaneko S., Akaike A. Lipolysaccharide-induced dopaminergic cell death in rat midbrain cultures: role of inducible nitric oxide synthase and protection by indomethacin. J. Neurochem. 2003, 86:1201-1212.
66. Shim S., Shuman M., Duncan E. An emerging role for cGMP in the treatment of schizophrenia: a review. Schizophr. Res. 2016, 170:226-231.
67. 3 excitotoxicity in the rat brain. Brain Res. Bull. 2010, 81:641-646.
68. Taneli F., Piridar S., Akdeniz F., Uyanik B.S., Ari Z. Serum nitric oxide metabolite levels and the effect of antipsychotic therapy in schizophrenia. Arch. Med. Res. 2004, 35:401-405.
69. Tran M.H., Yamada K., Nakajiama A., Mizuno M., He J., Kamei H., Nabeshima T. Tyrosine nitration of a synaptic protein synaptophysin contributes to amyloid β-peptide-induced cholinergic dysfunction. Mol. Psychiatry 2003, 8:407-412.
70. Trevlopoulou A., Touzlatzi N., Pitsikas N. The nitric oxide donor sodium nitroprusside attenuates recognition memory deficits and social withdrawal produced by the NMDA receptor antagonist ketamine and induces anxiolytic-like behaviour in rats. Psychopharmacology 2016, 233:1045-1054.
71. Tricklebank M.D., Singh L., Oles R.J., Preston C., Iversen S.D. The behavioural effects of MK-801: a comparison with antagonists acting non-competitively and competitively at the NMDA receptor. Eur. J. Pharmacol. 1989, 167:127-135.
72. Verma A., Moghaddam B. NMDA receptor antagonists impair prefrontal cortex function as assessed via spatial delayed alternation performance in rats: modulation by dopamine. J. Neurosci. 1996, 16:373-379.
73. Vijayraghavan S., Wang M., Birnbaum S.G., Williams G.V., Arnsten A.F. Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory. Nat. Neurosci. 2007, 10:376-384.
74. Wang Q., Rowan M.J., Anwyl R. Beta-amyloid-mediated inhibition of NMDA receptor-dependent long-term potentiation induction involves activation of microglia and stimulation of inducible nitric oxide synthase and superoxide. J. Neurosci. 2004, 24:6049-6056.
75. Wass C., Archer T., Palsson E., Fejgin K., Klamer D., Engel J.A., Svensson L. Effects of phencyclidine on spatial learning and memory: nitric oxide-dependent mechanisms. Behav. Brain Res. 2006, 171:147-153.
76. Wass C., Archer T., Palsson E., Fejgin K., Alexandersson A., Klamer D., Engel J.A., Svensson L. Phencyclidine affects memory in a nitric oxide-dependent manner: working and reference memory. Behav. Brain Res. 2006, 174:49-55.
77. Wass C., Klamer D., Fejgin K., Palsson E. The importance of nitric oxide in social dysfunction. Behav. Brain Res. 2009, 200:113-116.
78. Yamada K., Komori Y., Tanaka T., Senzaki K., Nikai T., Sugihara H., Kameyama T., Nabeshima T. Brain dysfunction associated with an induction of nitric oxide synthase following an intracerebral injection of lipopolysaccharide in rats. Neuroscience 1999, 88:281-294.
79. Yilmaz N., Herken H., Cicek H.K., Celik A., Yurekli M., Akyol O. Increased levels of nitric oxide, cortisol and adrenomedullin in patients with chronic schizophrenia. Med. Princ. Pract. 2007, 16:137-141.
80. Zhu F., Liu V., Zhao J., Zheng Y. Minocycline alleviates behavioral deficits and inhibits microglial activation induced by intrahippocampal administration of granulocyte-macrophage colony-stimulating factor in adult rats. Neurobiologia 2014, 266:275-281.
81. Zhu F., Zhang X., Ding Y.Q., Zhao J., Zheng Y. Neonatal intrahippocampal injection of lipolysaccharide induces deficits in social behavior and prepulse inhibition and microglial activation in rats: implication for a new schizophrenia animal model. Brain Behav. Immun. 2014, 38:166-174.