Nitric oxide-mediated anxiolytic-like and antidepressant-like effects in animal models of anxiety and depression

Pharmacology Biochemistry and Behavior

Volumn 88, Issue 3, 2008, Pages 247-255

  Spiacci Jr , A ^a   Kanamaru, F ^a   Guimaraes F S ^b   Oliveira, R M W ^a  

^a STATE UNIVERSITY OF MARINGÁ   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Dorsal raphe nucleus; Elevated plus maze; Forced swim test; Nitric oxide

Indexed keywords

7 NITROINDAZOLE; 8 BROMO CYCLIC GMP; ARGININE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; CONTROLLED STUDY; DEPRESSION; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; DRUG MEGADOSE; LOCOMOTION; LOW DRUG DOSE; MALE; MAZE TEST; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT; SWIMMING; TRANQUILIZING ACTIVITY;

ANIMALS; ANTI-ANXIETY AGENTS; ANTIDEPRESSIVE AGENTS; ANXIETY; ARGININE; DEPRESSION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; INDAZOLES; MALE; MOTOR ACTIVITY; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; RAPHE NUCLEI; RATS; RATS, WISTAR; SWIMMING; SYNAPTIC TRANSMISSION;

ANIMALIA; RATTUS;

EID: 36248959331     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbb.2007.08.008     Document Type: Article

References (73)

1. Abrams J., Johnson P., Hollis J., and Lowry C. Anatomic and functional topography of the dorsal raphe nucleus. Ann N Y Acad Sci 1018 (2004) 46-57
2. Bishop C., Tessmer J., Ullrich T., Rice K., and Walker P. Serotonin 5-HT2A receptors underlie increased motors behaviors induced in dopamine-depleted rats by intrastriatal 5-HT2A/2C agonism. J Pharmacol Exp Ther 310 (2004) 687-694
3. Campbell J., Fogarty J., and Spear L. Inhibition of nitric oxide synthesis with l-LAME suppresses isolation-induced ultrasounds in rat pups. Pharmacol Biochem Behav 63 (1999) 45-53
4. Cappendijk S., Duval S., de Vries R., and Dzoljic M. Comparative study of normotensive and hypertensive nitric oxide synthase inhibitors on morphine withdrawal syndrome in rats. Neurosci Lett 183 (1995) 67-70
5. Carobrez A., and Bertoglio L. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev 29 (2005) 1193-1205
6. Celada P., Puig M., Casanovas J., Guillazo G., and Artigas F. Control of dorsal raphe serotonergic neurons by the medial prefrontal cortex: involvement of serotonin-1A, GABA-A, and glutamate receptors. J Neurosci 21 (2001) 9917-9929
7. Chaparro-Huerta V., Beas-Zarate C., Guerrero M., and Feria-Velasco A. Nitric oxide involvement in regulating the dopamine transport in the striatal region of rat brain. Neurochem Int 31 (1997) 607-616
8. Contestabile A. Roles of NMDA receptor activity and nitric oxide production in brain development. Brain Res Brain Res Rev 32 (2000) 476-509
9. Czech DA Jacobson E., LeSueur-Reed K., and Kazel M. Putative anxiety-linked effects of the nitric oxide inhibitor l-NAME in three murine exploratory behavior models. Pharmacol Biochem Behav 75 (2003) 741-748
10. Da Silva G., Matteussi A., dos Santos A., Calixto J., and Rodrigues A. Evidence for dual effects of nitric oxide in the forced swimming test and in the tail suspension test in mice. NeuroReport 11 (2000) 3699-3702
11. Dall'Igna O., Dietrich M., Hoffman A., Neto W., Vendite D., Souza D., et al. Catalepsy ad hypolocomotion induced y nitric oxide donor: attenuation by theophylline. Eur J Pharmacol 432 (2001) 29-33
12. De Oliveira C., Del Bel E., and Guimarães F. Effects of l-NOARG on plus-maze performance in rats. Pharmacol Biochem Behav 56 (1997) 55-59
13. De Oliveira R., Del Bel E., and Guimarães F. Effects of excitatory amino acids and nitric oxide on flight behavior elicited from the dorsolateral periaqueductal gray. Neurosci Biobehav Rev 25 (2001) 679-685
14. Del Bel E., Guimarães F., Bermudez-Echeverry M., Gomez M., Schiaveto de Souza A., Padovan-Neto F., et al. Role of nitric oxide on motor behavior. Cell Mol Neurobiol 25 (2005) 371-392
15. Del Bel E., Souza A., Guimarães F., Da Silva C., and Nucci da Silva L. Motor effects of acute and chronic inhibition of nitric oxide synthesis in mice. Psychopharmacology 161 (2002) 32-37
16. Dun N., Dun S., and Forstermann U. Nitric oxide synthase immunoreactivity in rat pontine medullary neurons. Neuroscience 59 (1994) 429-445
17. Dzoljic E., De Vries R., and Dzoljic M. New and potent inhibitors of nitric oxide synthase reduce motor activity in mice. Behav Brain Res 87 (1997) 209-212
18. Érgün Y., and Érgün U. Prevention of pro-depressant effect of l-arginine in the forced swim test by NG-nitro-l-arginine and [1H-[1,2,4]oxadiazole[4,3-a]quinoxalin-1-one]. Eur J Pharmacol 554 (2007) 150-154
19. Eroglu L., and Çaglayan B. Anxiolytic and antidepressant properties of methylene blue in animal models. Pharmacol Res 36 (1997) 381-385
20. Esplugues J. NO as a signalling molecule in the nervous system. Brit J Pharmacol 135 (2002) 1079-1095
21. Faria M., Muscara M., Moreno J., Teixeira S., Dias H., De Oliveira B., et al. Acute inhibition of nitric oxide synthesis induces anxiolysis in the plus maze test. Eur J Pharmacol 323 (1997) 37-43
22. File S. Factors controlling measures of anxiety and responses to novelty in the mouse. Behav Brain Res 125 (2001) 151-157
23. Forestiero D., Manfrim C., Guimarães F., and De Oliveira R. Anxiolytic-like effects induced by nitric oxide synthase inhibitors microinjected into the medial amygdala of rats. Psychopharmacology 184 (2006) 166-172
24. Garthwaite J., and Boulton C. Nitric oxide signaling in the central nervous system. Annu Rev Physiol 57 (1995) 683-706
25. Garthwaite J., Garthwaite G., Palmer R., and Moncada S. NMDA receptor activation induces nitric oxide synthesis from arginine in rat brain slices. Eur J Pharmacol 172 (1989) 413-416
26. Gonzalez L., Andrews N., and File S. 5-HT1A and bezodiazepine receptors in the basolateral amygdala modulate anxiety in the social interaction test, but not in the elevated plus-maze. Brain Res 732 (1996) 145-153
27. Graeff F., Guimarães F., De Andrade T., and Deakin J. Role of 5-HT in stress, anxiety, and depression. Pharmacol Biochem Behav 54 (1996) 129-141
28. Grahn R., Watkins L., and Maier S. Impaired escape performance and enhanced conditioned fear in rats following exposure to an uncontrollable stressor are mediated by glutamate and nitric oxide in the dorsal raphe nucleus. Behav Brain Res 112 (2000) 33-41
29. Griebel G. 5-Hydroxytryptamine-interacting drugs in animal models of anxiety disorders: more than 30 years of research. Pharmacol Ther 65 (1995) 319-395
30. Guimarães F., Beijamini V., Moreira F., Aguiar D., and de Lucca A. Role of nitric oxide in brain regions related to defensive reactions. Neurosci Biobehav Rev 29 (2005) 1313-1322
31. Guimarães F., De Aguiar J., Del Bel E., and Ballejo G. Anxiolytic effect of nitric oxide synthase inhibitors microinjected into the dorsal central grey. Neuroreport 5 (1994) 1929-1932
32. Harkin A., Connor T., Burns M., and Kelly J. Nitric oxide synthase inhibitors augment the effects of serotonin re-uptake inhibitors in the forced swimming test. Eur Neuropsychopharmacol 14 (2004) 274-281
33. Harkin A., Connor T., Walsh M., St. John N., and Kelly J. Serotonergic mediation of the antidepressant-like effects of nitric oxide synthase inhibitors. Neuropharmacology 44 (2003) 616-623
34. Harkin A., Bruce K., Craft B., and Paul I. Nitric oxide synthase inhibitors have antidepressant-like properties in mice. 1. Acute treatments are active in the forced swim test. Eur J Pharmacol 372 (1999) 207-213
35. Hecker M., Mitchell J., Harris H., Katsura M., Thiemermann C., and Vane J. Endothelial cells metabolize NG-monomethyl-l-arginine to l-citrulline and subsequently to l-arginine. Biochem Biophys Res Commun 167 (1990) 1037-1043
36. Heiberg I., Wegener G., and Rosenberg R. Reduction of cGMP and nitric oxide has antidepressant-like effects in the forced swimming test in rats. Behav Brain Res 134 (2002) 479-484
37. Inan S., Yalcin I., and Aksu F. Dual effects of nitric oxide in the mouse forced swimming test: possible contribution of nitric oxide-mediated serotonin release and potassium channel modulation. Pharmacol Biochem Behav 77 (2004) 457-464
38. Jacobs B., and Azmitia E. Structure and function of the brain serotonin system. Physiol Rev 72 (1992) 165-229
39. Jefferys D., and Funder J. Nitric oxide modulates retention of immobility in the forced swimming test in rats. Eur J Pharmacol 295 (1996) 131-135
40. Joca S., and Guimarães F. Inhibition of neuronal nitric oxide synthase in the rat hippocampus induces antidepressant-like effects. Psychopharmacology (Berl) 185 (2006) 298-305
41. Kaster M., Rosa A., Santos A., and Rodrigues A. Involvement of nitric oxide-cGMP pathway in the antidepressant-like effects of adenosine in the forced swimming test. Int J Neuropsychopharmacol 8 (2005) 601-606
42. Kriegsfeld L., Eliasson M., Demas G., Blackshaw S., Dawson T., Nelson R., et al. Nocturnal motor coordination deficits in neuronal nitric oxide synthase knock-out mice. Neuroscience 89 (1999) 311-315
43. Leza J-C Lizasoain I., Cuellar B., Moro M., and Lorenzo P. Correlation between brain nitric oxide synthase activity and opiate withdrawal. Naunyn-Schimiedeberg's Arch Pharmacol 353 (1996) 349-354
44. Lino-de-Oliveira C., De Lima T., and de Padua Carobrez A. Structure of the rat behaviour in the forced swimming test. Behav Brain Res 158 (2005) 243-250
45. Lovick T. Influence of the dorsal and median raphe nuclei on neurons in the periaqueductal gray matter: role of 5-hydroxytryptamine. Neuroscience 59 (1994) 993-1000
46. Lowry C., Johnson P., Hay-Schmidt A., Mikkelsen J., and Shekhar A. Modulation of anxiety circuits by serotonergic systems. Stress 8 (2005) 233-246
47. Lowry C. Functional subsets of serotonergic neurones: implications for control of the hypothalamic-pituitary-adrenal axis. J Neuroendocrinol 14 (2002) 911-923
48. Maier S., and Watkins L. Stressor controllability and learned helplessness: the roles of the dorsal raphe nucleus, serotonin, and corticotrophin-releasing factor. Neurosci Biobehav Rev 29 (2005) 829-841
49. Masood A., Banerjee B., Vijayan V., and Ray A. Modulation of stress-induced neurobehavioral changes by nitric oxide in rats. Eur J Pharmacol 458 (2003) 135-139
50. Monti J., Hantos H., Ponzoni A., Monti D., and Banchero P. Role of nitric oxide in sleep regulation: effects of l-NAME, an inhibitor of nitric oxide synthase, on sleep in rats. Behav Brain Res 100 (1999) 197-205
51. Monzon M., Varas M., and De Barioglio S. Anxiogenesis induced by nitric oxide synthase inhibition and anxiolytic effect of melanin-concentrating hormone (MCH) in rat brain. Peptides 22 (2001) 1043-1047
52. Noda Y., Yamada K., Furukawa H., and Nabeshima T. Involvement of nitric oxide in phencyclidine-induced hyperlocomotion in mice. Eur. J Pharmacol 286 (1995) 291-297
53. Onstott D., Mayer B., and Beitz A. Nitric oxide synthase immunoreactive neurons anatomically define a longitudinal dorsolateral column within the midbrain periaqueductal gray of the rat: analysis using laser confocal microscopy. Brain Res 610 (1993) 317-324
54. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates. 3rd ed (1997), Academic Press, San Diego
55. Pellow S., and File S. Anxiolytic and anxiogenic drug effects on exploratory activity n an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol Biochem Behav 24 (1986) 525-529
56. Porsolt R., Le Pichon M., and Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 266 (1977) 7302
57. Prast H., and Philippu A. Release of endogenous acetylcholine in the hypothalamus of conscious rats. Naunyn Schmiedebergs Arch Pharmacol 346 (1992) 1-3
58. Quock R., and Nguyen E. Possible involvement of nitric oxide in chlordiazepoxide-induced anxiolysis in mice. Life Sci 51 (1992) PL255-PL260
59. Sandi C., Venero C., and Guaza C. Decreased spontaneous motor activity and startle response in nitric oxide synthase inhibitor-treated rats. Eur J Pharmacol 277 (1995) 89-97
60. Schuman E., and Madison D. A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 254 (1991) 1503-1506
61. Segieth J., Fowler I., Whitton P., and Pearce B. Nitric oxide-mediated regulation of dopamine release in the hippocampus in vivo. Neuropharmacology 39 (2000) 571-577
62. Segieth J., Gerring S., Biggs C., and Whitton P. Nitric oxide regulates excitatory. Neurosci Lett 200 (1995) 101-104
63. Shin J., Chung S., Park E., Uhm D., and Suh C. Nitric oxide directly activates calcium-activated potassium channels from rat brain reconstituted into planar lipid bilayer. FEBS Lett 415 (1997) 299-302
64. Silva M., Rose S., Hindmarsh J., Jenner P., and Marsde C. l-arginine produces NO-independent increases in dopamine efflux in rat striatum. Neuroreport 9 (1997) 149-152
65. Simpson K., Waterhouse B., and Lin R. Differential expression of nitric oxide in serotonergic projection neurons: neurochemical identification of dorsal raphe inputs to rodent trigeminal somatosensory targets. J Comp Neurol 466 (2003) 495-512
66. Tagliaferro P., Ramos A., Lopez-Costa J., Lopez E., Saavedra J., and Brusco A. Increased nitric oxide synthase activity in a model of serotonin depletion. Brain Res Bull 54 (2001) 199-205
67. Volke V., Koks S., Vasar E., Bourin M., Bradwejn J., and Mannisto P. Inhibition of nitric oxide synthase causes anxiolytic-like behaviour in an elevated plus-maze. Neuroreport 6 (1995) 1413-1416
68. Volke V., Soosaar A., Koks S., Bourin M., Mannisto P., and Vasar E. 7-Nitroindazole, a nitric oxide synthase inhibitor, has anxiolytic-like properties in exploratory models of anxiety. Psychopharmacology (Berl) 131 (1997) 399-405
69. Volke V., Wegener G., Bourin M., and Vasar E. Antidepressant-and anxiolytic-like effects of selective neuronal NOS inhibitor 1-(2-trifluoromethylphenyl)-imidazole in mice. Behav Brain Res 140 (2003) 141-147
70. Volke V., Wegener G., and Vasar E. Augmentation of the NO-cGMP cascade induces anxiogenic-like effect in mice. J Physiol Pharmacol 54 (2003) 653-660
71. Wang Q., Guan J., and Nakai Y. Distribution and synaptic relations of NOS neurons in the dorsal raphe nucleus: a comparison to 5-HT neurons. Brain Res Bull 37 (1995) 177-187
72. Xu Z., and Hokfelt T. Expression of galanin and nitric oxide synthase in subpopulations of serotonin neurons of the rat dorsal raphe nucleus. J Chem Neuroanat 13 (1997) 169-187
73. Yildiz F., Erden B., Ulak G., Utkan T., and Gacar N. Antidepressant-like effect of 7-nitroindazole in the forced swimming test in rats. Psychopharmacology (Berl). 149 (2000) 41-44