Antidepressant-like effect of nitric oxide synthase inhibitors and sildenafil against lipopolysaccharide-induced depressive-like behavior in mice

Neuroscience

Volumn 268, Issue , 2014, Pages 236-246

  Tomaz, V S ^a   Cordeiro, R C ^a   Costa, A M N ^a   De Lucena, D F ^a   Nobre Junior H V ^a   De Sousa, F C F ^a   Vasconcelos, S M M ^a   Vale, M L ^a   Quevedo, J ^b,c   Macedo D ^a  

^a FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^b UNIVERSITY OF SOUTHERN SANTA CATARINA   (Brazil)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

BDNF; Depressive like behavior; LPS; Neuroinflammation; Nitric oxide; Oxidative stress

Indexed keywords

AMINOGUANIDINE; ARGININE; BRAIN DERIVED NEUROTROPHIC FACTOR; GLUTATHIONE; IMIPRAMINE; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; N(G) NITROARGININE METHYL ESTER; SILDENAFIL; ANTIDEPRESSANT AGENT; CYCLIC GMP; ENZYME INHIBITOR; GUANIDINE DERIVATIVE; IL1B PROTEIN, MOUSE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PIPERAZINE DERIVATIVE; PURINE DERIVATIVE; SULFONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIDEPRESSANT ACTIVITY; ARTICLE; BRAIN LEVEL; CONTROLLED STUDY; CORPUS STRIATUM; DEPRESSION; FORCED SWIM TEST; HIPPOCAMPUS; LIPID PEROXIDATION; LOCOMOTION; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PREFRONTAL CORTEX; PREPULSE INHIBITION; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SUCROSE PREFERENCE TEST; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; DEPRESSIVE DISORDER; DISEASE MODEL; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTIDEPRESSIVE AGENTS; ARGININE; BEHAVIOR, ANIMAL; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CYCLIC GMP; DEPRESSIVE DISORDER; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; GUANIDINES; IMIPRAMINE; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MALE; MICE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXIDATIVE STRESS; PIPERAZINES; PURINES; SIGNAL TRANSDUCTION; SULFONES;

EID: 84897521185     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.03.025     Document Type: Article

References (71)

1. Ainscough E.W., Brodie A.M. Nitric oxide-some old and new perspectives. J Chem Educ 1995, 72.
2. Akira S., Takeda K. Toll-like receptor signalling. Nat Rev Immunol 2004, 4:499-511.
3. Alderton W.K., Cooper C.E., Knowles R.G. Nitric oxide synthases: structure, function and inhibition. Biochem J 2001, 357:593-615.
4. Archer J. Tests for emotionality in rats and mice: a review. Anim Behav 1973, 21:205-235.
5. Bakish D. New standard of depression treatment: remission and full recovery. J Clin Psychiatry 2001, 26:5-9.
6. Bettio L.E., Cunha M.P., Budni J., Pazini F.L., Oliveira A., Colla A.R., Rodrigues A.L. Guanosine produces an antidepressant-like effect through the modulation of NMDA receptors, nitric oxide-cGMP and PI3K/mTOR pathways. Behav Brain Res 2012, 234:137-148.
7. Bilici M., Efe H., Koroglu M.A., Uydu H.A., Bekaroglu M., Deger O. Antioxidative enzyme activities and lipid peroxidation in major depression: alterations by antidepressant treatments. J Affect Disord 2001, 64:43-51.
8. Blaszczyk J.W., Tajchert K., Lapo I., Sadowski B. Acoustic startle and open-field behavior in mice bred for magnitude of swim analgesia. Physiol Behav 2000, 70:471-476.
9. Brunoni A.R., Lopes M., Fregni F. A systematic review and meta-analysis of clinical studies on major depression and BDNF levels: implications for the role of neuroplasticity in depression. Int J Neuropsychopharmacol 2008, 11:1169-1180.
10. Calabrese V., Mancuso C., Calvani M., Rizzarelli E., Butterfield D.A., Stella A.M. Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat Rev Neurosci 2007, 8:766-775.
11. Carvalho L.A., Torre J.P., Papadopoulos A.S., Poon L., Juruena M.F., Markopoulou K., Cleare A.J., Pariante C.M. Lack of clinical therapeutic benefit of antidepressants is associated overall activation of the inflammatory system. J Affect Disord 2013, 148:136-140.
12. Custodio C.S., Mello B.S., Cordeiro R.C., de Araujo F.Y., Chaves J.H., Vasconcelos S.M., Nobre Junior H.V., de Sousa F.C., Vale M.L., Carvalho A.F., Macedo D.S. Time course of the effects of lipopolysaccharide on prepulse inhibition and brain nitrite content in mice. Eur J Pharmacol 2013, 713:31-38.
13. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 2008, 9:46-56.
14. De La Garza Ii R. Endotoxin- or pro-inflammatory cytokine-induced sickness behavior as an animal model of depression: focus on anhedonia. Neurosci Biobehav Rev 2005, 29:761-770.
15. DellaGioia N., Devine L., Pittman B., Hannestad J. Bupropion pre-treatment of endotoxin-induced depressive symptoms. Brain Behav Immun 2013, 31:197-204.
16. Dhir A., Kulkarni S.K. Involvement of l-arginine-nitric oxide-cyclic guanosine monophosphate pathway in the antidepressant-like effect of venlafaxine in mice. Prog Neuro-Psychopharmacol Biol Psychiatry 2007, 31:921-925.
17. Draper H.H., Squires E.J., Mahmoodi H., Wu J., Agarwal S., Hadley M. A comparative evaluation of thiobarbituric acid methods for the determination of malondialdehyde in biological materials. Free Radic Biol Med 1993, 15:353-363.
18. Ellman G.L. Tissue sulfhydryl groups. Arch Biochem Biophys 1959, 82:70-77.
19. Fanous S., Hammer R.P., Nikulina E.M. Short- and long-term effects of intermittent social defeat stress on brain-derived neurotrophic factor expression in mesocorticolimbic brain regions. Nat Rev Neurosci 2010, 167:598-607.
20. Ferreira Mello B.S., Monte A.S., McIntyre R.S., Soczynska J.K., Custodio C.S., Cordeiro R.C., Chaves J.H., Mendes Vasconcelos S.M., Nobre Junior H.V., Florenco de Sousa F.C., Hyphantis T.N., Carvalho A.F., Macedo D.S. Effects of doxycycline on depressive-like behavior in mice after lipopolysaccharide (LPS) administration. J Psychiatr Res 2013, 47:1521-1529.
21. Feyissa A.M., Chandran A., Stockmeier C.A., Karolewicz B. Reduced levels of NR2A and NR2B subunits of NMDA receptor and PSD-95 in the prefrontal cortex in major depression. Prog Neuro-Psychopharmacol Biol Psychiatry 2009, 33:70-75.
22. Garate I., Garcia-Bueno B., Madrigal J.L., Bravo L., Berrocoso E., Caso J.R., Mico J.A., Leza J.C. Origin and consequences of brain Toll-like receptor 4 pathway stimulation in an experimental model of depression. J Neuroinflamm 2011, 8:1742-2094.
23. Gardner A., Johansson A., Wibom R., Nennesmo I., von Dobeln U., Hagenfeldt L., Hallstrom T. Alterations of mitochondrial function and correlations with personality traits in selected major depressive disorder patients. J Affect Disord 2003, 76:55-68.
24. Gomes C., Ferreira R., George J., Sanches R., Rodrigues D.I., Goncalves N., Cunha R.A. Activation of microglial cells triggers a release of brain-derived neurotrophic factor (BDNF) inducing their proliferation in an adenosine A2A receptor-dependent manner: A2A receptor blockade prevents BDNF release and proliferation of microglia. J Neuroinflamm 2013, 10:1742-2094.
25. Grigoleit J.S., Kullmann J.S., Wolf O.T., Hammes F., Wegner A., Jablonowski S., Engler H., Gizewski E., Oberbeck R., Schedlowski M. Dose-dependent effects of endotoxin on neurobehavioral functions in humans. PLoS One 2011, 6:2.
26. Gururajan A., Taylor D.A., Malone D.T. Effect of testing conditions on the propsychotic action of MK-801 on prepulse inhibition, social behaviour and locomotor activity. Physiol Behav 2010, 99:131-138.
27. Heydarpour P., Salehi-Sadaghiani M., Javadi-Paydar M., Rahimian R., Fakhfouri G., Khosravi M., Khoshkish S., Gharedaghi M.H., Ghasemi M., Dehpour A.R. Estradiol reduces depressive-like behavior through inhibiting nitric oxide/cyclic GMP pathway in ovariectomized mice. Horm Behav 2013, 63:361-369.
28. Hoshino K., Takeuchi O., Kawai T., Sanjo H., Ogawa T., Takeda Y., Takeda K., Akira S. Cutting edge: toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 1999, 162:3749-3752.
29. Joca S., Guimarães F. Inhibition of neuronal nitric oxide synthase in the rat hippocampus induces antidepressant-like effects. Eur Neuropsychopharmacol 2006, 185:298-305.
30. Kaviani H., Gray J.A., Checkley S.A., Raven P.W., Wilson G.D., Kumari V. Affective modulation of the startle response in depression: influence of the severity of depression, anhedonia, and anxiety. J Affect Disord 2004, 83:21-31.
31. Kim E.J., Kwon K.J., Park J.-Y., Lee S.H., Moon C.-H., Baik E.J. Effects of peroxisome proliferator-activated receptor agonists on LPS-induced neuronal death in mixed cortical neurons: associated with iNOS and COX-2. Behav Brain Res 2002, 941:1-10.
32. Kubera M., Curzytek K., Duda W., Leskiewicz M., Basta-Kaim A., Budziszewska B., Roman A., Zajicova A., Holan V., Szczesny E., Lason W., Maes M. A new animal model of (chronic) depression induced by repeated and intermittent lipopolysaccharide administration for 4 months. Brain Behav Immun 2013, 31:96-104.
33. Lejuez C.W., Hopko D.R., Acierno R., Daughters S.B., Pagoto S.L. Ten year revision of the brief behavioral activation treatment for depression: revised treatment manual. Behav Modif 2011, 35:111-161.
34. Leonard B., Maes M. Mechanistic explanations how cell-mediated immune activation, inflammation and oxidative and nitrosative stress pathways and their sequels and concomitants play a role in the pathophysiology of unipolar depression. Neurosci Biobehav Rev 2012, 36:764-785.
35. Levine J., Barak Y., Chengappa K.N., Rapoport A., Rebey M., Barak V. Cerebrospinal cytokine levels in patients with acute depression. Neuropsychobiology 1999, 40:171-176.
36. Ludka F.K., Zomkowski A.D., Cunha M.P., Dal-Cim T., Zeni A.L., Rodrigues A.L., Tasca C.I. Acute atorvastatin treatment exerts antidepressant-like effect in mice via the l-arginine-nitric oxide-cyclic guanosine monophosphate pathway and increases BDNF levels. Eur Neuropsychopharmacol 2013, 23:400-412.
37. Maes M. Major depression and activation of the inflammatory response system. Adv Exp Med Biol 1999, 461:25-46.
38. Maes M., Meltzer H.Y., Scharpe S., Bosmans E., Suy E., De Meester I., Calabrese J., Cosyns P. Relationships between lower plasma l-tryptophan levels and immune-inflammatory variables in depression. Psychiatry Res 1993, 49:151-165.
39. Maes M., Scharpe S., Meltzer H.Y., Okayli G., Bosmans E., D'Hondt P., Vanden Bossche B.V., Cosyns P. Increased neopterin and interferon-gamma secretion and lower availability of l-tryptophan in major depression: further evidence for an immune response. Psychiatry Res 1994, 54:143-160.
40. Maes M., Vandoolaeghe E., Neels H., Demedts P., Wauters A., Meltzer H.Y., Altamura C., Desnyder R. Lower serum zinc in major depression is a sensitive marker of treatment resistance and of the immune/inflammatory response in that illness. Prog Neuro-Psychopharmacol Biol Psychiatry 1997, 42:349-358.
41. Maes M., Kubera M., Leunis J.C. The gut-brain barrier in major depression: intestinal mucosal dysfunction with an increased translocation of LPS from gram negative enterobacteria (leaky gut) plays a role in the inflammatory pathophysiology of depression. Neuro Endocrinol Lett 2008, 29:117-124.
42. Maes M., Galecki P., Chang Y.S., Berk M. A review on the oxidative and nitrosative stress (O&NS) pathways in major depression and their possible contribution to the (neuro)degenerative processes in that illness. Prog Neuro-Psychopharmacol Biol Psychiatry 2011, 35:676-692.
43. Mao Q.Q., Huang Z., Zhong X.M., Xian Y.F., Ip S.P. Brain-derived neurotrophic factor signalling mediates the antidepressant-like effect of piperine in chronically stressed mice. Behav Brain Res 2014, 261:140-145.
44. McNally L., Bhagwagar Z., Hannestad J. Inflammation, glutamate, and glia in depression: a literature review. CNS Spectr 2008, 13:501-510.
45. Montezuma K., Biojone C., Lisboa S.F., Cunha F.Q., Guimaraes F.S., Joca S.R. Inhibition of iNOS induces antidepressant-like effects in mice: pharmacological and genetic evidence. Neuropharmacology 2012, 62:485-491.
46. Moreno-Lopez B., Gonzalez-Forero D. Nitric oxide and synaptic dynamics in the adult brain: physiopathological aspects. Rev Neurosci 2006, 17:309-357.
47. Munhoz C.D., Lepsch L.B., Kawamoto E.M., Malta M.B., Lima Lde S., Avellar M.C., Sapolsky R.M., Scavone C. Chronic unpredictable stress exacerbates lipopolysaccharide-induced activation of nuclear factor-kappaB in the frontal cortex and hippocampus via glucocorticoid secretion. J Neurosci 2006, 26:3813-3820.
48. Ohgi K., Kajiya H., Okamoto F., Nagaoka Y., Onitsuka T., Nagai A., Sakagami R., Okabe K. A novel inhibitory mechanism of nitrogen-containing bisphosphonate on the activity of Cl(-) extrusion in osteoclasts. Naunyn Schmiedebergs Arch Pharmacol 2013, 386:589-598.
49. Perry W., Minassian A., Feifel D. Prepulse inhibition in patients with non-psychotic major depressive disorder. J Affect Disord 2004, 81:179-184.
50. Porsolt R.D., Le Pichon M., Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nat Rev Neurosci 1977, 266:730-732.
51. Prast H., Philippu A. Nitric oxide as modulator of neuronal function. Prog Neurobiol 2001, 64:51-68.
52. Resources IoLA Guide for the care and used of laboratory animals 1996, National Academies Press.
53. Ribeiro D.E., Maiolini V.M., Soncini R., Antunes-Rodrigues J., Elias L.L., Vilela F.C., Giusti-Paiva A. Inhibition of nitric oxide synthase accentuates endotoxin-induced sickness behavior in mice. Pharmacol Biochem Behav 2013, 103:535-540.
54. Rosa J.M., Dafre A.L., Rodrigues A.L. Antidepressant-like responses in the forced swimming test elicited by glutathione and redox modulation. Behav Brain Res 2013, 253:165-172.
55. Rush A.J., Wisniewski S.R., Zisook S., Fava M., Sung S.C., Haley C.L., Chan H.N., Gilmer W.S., Warden D., Nierenberg A.A., Balasubramani G.K., Gaynes B.N., Trivedi M.H., Hollon S.D. Is prior course of illness relevant to acute or longer-term outcomes in depressed out-patients? A STAR*D report. Psychol Med 2012, 42:1131-1149.
56. Russell J.A., Douglas A.J., Brunton P.J. Reduced hypothalamo-pituitary-adrenal axis stress responses in late pregnancy: central opioid inhibition and noradrenergic mechanisms. Ann N Y Acad Sci 2008, 1148:428-438.
57. Rygula R., Abumaria N., Flügge G., Fuchs E., Rüther E., Havemann-Reinecke U. Anhedonia and motivational deficits in rats: impact of chronic social stress. Behav Brain Res 2005, 162:127-134.
58. Sayre L.M., Perry G., Smith M.A. Oxidative stress and neurotoxicity. Chem Res Toxicol 2007, 21:172-188.
59. Şeneş M., Kazan N., Coşkun Ö., Zengi O., Inan L., Yücel D. Oxidative and nitrosative stress in acute ischaemic stroke. Ann Clin Biochem 2007, 44:43-47.
60. Socala K., Nieoczym D., Wyska E., Poleszak E., Wlaz P. Sildenafil, a phosphodiesterase type 5 inhibitor, enhances the activity of two atypical antidepressant drugs, mianserin and tianeptine, in the forced swim test in mice. Prog Neuro-Psychopharmacol Biol Psychiatry 2012, 38:121-126.
61. Swerdlow N.R., Geyer M.A. Prepulse inhibition of acoustic startle in rats after lesions of the pedunculopontine tegmental nucleus. Behav Neurosci 1993, 107:104-117.
62. Taylor M.J., Rudkin L., Bullemor-Day P., Lubin J., Chukwujekwu C., Hawton K. Strategies for managing sexual dysfunction induced by antidepressant medication. Cochrane Database Syst Rev 2013, 31.
63. Teasdale J.D. Negative thinking in depression: cause, effect, or reciprocal relationship?. Adv Behav Res Ther 1983, 5:3-25.
64. Tejeda H., Chefer V., Zapata A., Shippenberg T. The effects of kappa-opioid receptor ligands on prepulse inhibition and CRF-induced prepulse inhibition deficits in the rat. Eur Neuropsychopharmacol 2010, 210:231-240.
65. Tsigos C., Chrousos G.P. Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. J Psychosom Res 2002, 53:865-871.
66. Vasconcelos Rios E.R., Moura Rocha N.F., Rodrigues Carvalho A.M., Freire Vasconcelos L., Leite Dias M., de Carvalho Lima C.N., Soares Lopes K., Cavalcante Melo F.H., de Franca Fonteles M.M. Involvement of the nitric oxide/cyclic guanylate monophosphate pathway in the pilocarpine-induced seizure model in mice. Eur J Pharmacol 2013, 91:131-134.
67. Wang X., Robinson P.J. Cyclic GMP-dependent protein kinase and cellular signaling in the nervous system. J Neurochem 1997, 68:443-456.
68. Zarate C.A., Singh J.B., Carlson P.J., et al. A randomized trial of an n-methyl-d-aspartate antagonist in treatment-resistant major depression. Arch Gen Psychiatry 2006, 63:856-864.
69. Zhang G.F., Wang N., Shi J.Y., Xu S.X., Li X.M., Ji M.H., Zuo Z.Y., Zhou Z.Q., Yang J.J. Inhibition of the l-arginine-nitric oxide pathway mediates the antidepressant effects of ketamine in rats in the forced swimming test. Pharmacol Biochem Behav 2013, 24:8-12.
70. Zhou Q.-G., Hu Y., Hua Y., Hu M., Luo C.-X., Han X., Zhu X.-J., Wang B., Xu J.-S., Zhu D.-Y. Neuronal nitric oxide synthase contributes to chronic stress-induced depression by suppressing hippocampal neurogenesis. J Neurochem 2007, 103:1843-1854.
71. Zlatkovic J., Filipovic D. Chronic social isolation induces NF-kappaB activation and upregulation of iNOS protein expression in rat prefrontal cortex. Neurochem Int 2013, 63:172-179.