Inducible nitric oxide synthase is involved in the modulation of depressive behaviors induced by unpredictable chronic mild stress

Journal of Neuroinflammation

Volumn 9, Issue , 2012, Pages

  Peng, Yun Li ^a   Liu, Yu Ning ^a   Liu, Lei ^a   Wang, Xia ^a   Jiang, Chun Lei ^a   Wang, Yun Xia ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Depressive behavior; Inducible nitric oxide synthase; Unpredictable chronic mild stress

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; NITRITE; SUCROSE;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CELL; CELL DAMAGE; CHRONIC MILD STRESS; CONTROLLED STUDY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MAJOR DEPRESSION; MALE; MOUSE; NERVE DEGENERATION; NISSL SUBSTANCE; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; REST; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRESS;

EID: 84860194760     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-9-75     Document Type: Article

References (55)

1. Garciá-Bueno B, Caso JR, Leza JC. Stress as a neuroinflammatory condition in brain: damaging and protective mechanisms. Neurosci Biobehav Rev 2008, 32:1136-1151. 10.1016/j.neubiorev.2008.04.001, 18468686.
2. Lucas SM, Rothwell NJ, Gibson RM. The role of inflammation in CNS injury and disease. Br J Pharmacol 2006, 147:232-240.
3. WHO Mental Health, Depression 2010, WHO, Geneva, WHO.
4. van Amsterdam JGC, Opperhuizen A. Nitric oxide and biopterin in depression and stress. Psychiatry Res 1999, 85:33-38. 10.1016/S0165-1781(98)00140-1, 10195314.
5. Zhou L, Zhu DY. Neuronal nitric oxide synthase: structure, subcellular localization, regulation, and clinical implications. Nitric Oxide 2009, 20:223-230. 10.1016/j.niox.2009.03.001, 19298861.
6. de Vente J, Hopkins D, Van Markerink IM, Emson PC, Schmidt HH, Steinbusch HW. Distribution of nitric oxide synthase and nitric oxide-receptive, cyclic GMP-producing structures in the rat brain. Neuroscience 1998, 87:207-241. 10.1016/S0306-4522(98)00171-7, 9722153.
7. Dhir A, Kulkarni SK. Involvement of nitric oxide (NO) signaling pathway in the antidepressant action of bupropion, a dopamine reuptake inhibitor. Eur J Pharmacol 2007, 568:177-185. 10.1016/j.ejphar.2007.04.028, 17509558.
8. Heiberg IL, Wegener G, Rosenberg R. Reduction of cGMP and nitric oxide has antidepressant-like effects in the forced swimming test in rats. Behav Brain Res 2002, 134:479-484. 10.1016/S0166-4328(02)00084-0, 12191834.
9. Joca SR, Guimaraes FS. Inhibition of neuronal nitric oxide synthase in the rat hippocampus induces antidepressant-like effects. Psychopharmacology 2006, 185:298-305. 10.1007/s00213-006-0326-2, 16518647.
10. Volke V, Wegener G, Bourin M, Vasar E. Antidepressant- and anxiolytic-like effects of selective neuronal NOS inhibitor 1-(2-trifluoromethylphenyl)-imidazole in mice. Behav Brain Res 2003, 140:141-147. 10.1016/S0166-4328(02)00312-1, 12644287.
11. Adler UC, Marques AH, Calil HM. Inflammatory aspects of depression. Inflamm Allergy Drug Targets 2008, 7:19-23. 10.2174/187152808784165216, 18473896.
12. Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 2008, 9:46-56. 10.1038/nrn2297, 2919277, 18073775.
13. Dantzer R, Capuron L, Irwin MR, Miller AH, Ollat H, Perry VH, Rousey S, Yirmiya R. Identification and treatment of symptoms associated with inflammation in medically ill patients. Psychoneuroendocrinology 2008, 33:18-29. 10.1016/j.psyneuen.2007.10.008, 2234599, 18061362.
14. Das UN. Is depression a low-grade systemic inflammatory condition?. Am J Clin Nutr 2007, 85:1665-1666.
15. Raison CL, Capuron L, Miller AH. Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol 2006, 27:24-31. 10.1016/j.it.2005.11.006, 16316783.
16. Kemeny ME, Schedlowski M. Understanding the interaction between psychosocial stress and immunerelated diseases: a stepwise progression. Brain Behav Immun 2007, 21:1009-1018. 10.1016/j.bbi.2007.07.010, 17889502.
17. Campbell S, MacQueen G. Role of the hippocampus in the pathophysiology of major depression. J Psychiatry Neurosci 2004, 29:417-426. 524959, 15644983.
18. Grippo AJ, Moffitt JA, Johnson AK. Evaluation of baroreceptor reflex function in the chronic mild stress rodent model of depression. Psychosom Med 2008, 70:435-443. 10.1097/PSY.0b013e31816ff7dd, 18480191.
19. Wang W, Zolty E, Falk S, Summer S, Zhou Z, Gengaro P, Faubel S, Alo N, Channon K, Schrier R. Endotoxemia-related acute kidney injury in transgenic mice with endothelial over expression of GTP cyclohydrolase-1. Am J Physiol Renal Physiol 2008, 294:571-576.
20. Grippo AJ, Cushing BS, Carter CS. Depression-like behavior and stressor-induced neuroendocrine activation in female prairie voles exposed to chronic social isolation. Psychosom Med 2007, 69:149-157. 10.1097/PSY.0b013e31802f054b, 3006075, 17289829.
21. Tiziana R, Daniela V, Natalia R, Cinzia G, Daniela B, Valeria C, Chiara C, Francesca C, Patrizia R, Sanzio C, Mariaelvina S, Daniela P. Chronic Δ9-tetrahydrocannabinol during adolescence provokes sex-dependent changes in the emotional profile in adult rats: behavioral and biochemical correlates. Neuropsychopharmacology 2008, 33:2760-2771. 10.1038/sj.npp.1301664, 18172430.
22. Engeland CG, Kavaliers M, Ossenkopp KP. Sex differences in the effects of muramyl dipeptide and lipopolysaccharide on locomotor activity and the development of behavioral tolerance in rats. Pharmacol Biochem Behav 2003, 74:433-447. 10.1016/S0091-3057(02)01024-9, 12479965.
23. Reneric JP, Bouvard M, Stinus L. In the rat forced swimming test, chronic but not subacute administration of dual 5-HT/NA antidepressant treatments may produce greater effects than selective drugs. Behav Brain Res 2002, 136:521-532. 10.1016/S0166-4328(02)00203-6, 12429415.
24. Santiago RM, Barbieiro J, Lima MMS, Dombrowski PA, Andreatini R, Vital MABF. Depressive-like behaviors alterations induced by intranigral MPTP, 6-OHDA, LPS and rotenone models of Parkinson's disease are predominantly associated with serotonin and dopamine. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:1104-1114. 10.1016/j.pnpbp.2010.06.004, 20547199.
25. Flodström M, Tyrberg B, Eizirik DL, Sandler S. Reduced sensitivity of inducible nitric oxide synthase-deficient mice to multiple low-dose streptozotocin-induced diabetes. Diabetes 1999, 48:706-713. 10.2337/diabetes.48.4.706, 10102685.
26. Stein-Behrens B, Mattson MP, Chang I, Yeh M, Sapolsky R. Stress exacerbates neuron loss and cytoskeletal pathology in the hippocampus. J Neurosci 1994, 74:5373-5380.
27. Cai JM, Kang ZM, Liu K, Liu WW, Li RP, Zhang JH, Luo X, Sun XJ. Neuroprotective effects of hydrogen saline in neonatal hypoxia-ischemia rat model. Brain Res 2009, 1256:129-137.
28. Bechtholt AJ, Smith K, Gaughan S, Lucki I. Sucrose intake and fasting glucose levels in 5-HT(1A) and 5-HT(1B) receptor mutant mice. Physiol Behav 2008, 93:659-665. 10.1016/j.physbeh.2007.11.006, 2366078, 18155098.
29. Krishnan V, Han M-H, Graham DL, Berton O, Renthal W, Russo SJ, Laplant Q, Graham A, Lutter M, Lagace DC, Ghose S, Reister R, Tannous P, Green TA, Neve RL, Chakraverty S, Kumar A, Eisch AJ, Self DW, Lee FS, Tamminga CA, Cooper DC, Gershenfeld HK, Nestler EJ. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 2007, 131:391-404. 10.1016/j.cell.2007.09.018, 17956738.
30. Petit-Demouliere B, Chenu F, Bourin M. Forced swimming test in mice: a review of antidepressant activity. Psychopharmacology 2005, 177:245-255. 10.1007/s00213-004-2048-7, 15609067.
31. Drossopoulou G, Antoniou K, Kitraki E, Papathanasiou G, Papalexi E, Dalla C, Papadopoulou-Daifoti Z. Sex differences in behavioral, neurochemical and neuroendocrine effects induced by the forced swim test in rats. Neuroscience 2004, 126:849-857. 10.1016/j.neuroscience.2004.04.044, 15207320.
32. Porsolt RD, Le-Pichon M, Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977, 266:730-732. 10.1038/266730a0, 559941.
33. Suzuki E, Yagi G, Nakaki T, Kanba S, Asai M. Elevated plasma nitrate levels in depressive states. J Affect Disord 2001, 63:221-224. 10.1016/S0165-0327(00)00164-6, 11246099.
34. Angulo J, Peiró C, Sanchez-Ferrer CF, Gabancho S, Cuevas P, Gupta S, Tejada IS. Differential effects of serotonin reuptake inhibitors on erectile responses, NO-production, and neuronal NO synthase expression in rat corpus cavernosum tissue. Br J Pharmacol 2001, 134:1190-1194. 10.1038/sj.bjp.0704351, 1573043, 11704638.
35. Harvey BH, Retief R, Korff A, Wegener G. Increased hippocampal nitric oxide synthase activity and stress responsiveness after imipramine discontinuation: role of 5HT2A/C-receptors. Metab Brain Dis 2006, 21:211-220. 10.1007/s11011-006-9014-5, 16865538.
36. Zhou QG, Hu Y, Hua Y, Hu M, Luo CX, Han X, Zhu XJ, Wang B, Xu JS, Zhu DY. Neuronal nitric oxide synthase contributes to chronic stress-induced depression by suppressing hippocampal neurogenesis. J Neurochem 2007, 103:12.
37. Harkin A, Connor TJ, Walsh M, John NS, Kelly JP. Serotonergic mediation of the antidepressant-like effects of nitric oxide inhibitors. Neuropharmacology 2003, 44:1843-1854.
38. Mutlu O, Ulak G, Laugeray A, Belzung C. Effects of neuronal and inducible NOS inhibitor 1-[2-(trifluoromethyl) phenyl] imidazole (TRIM) in unpredictable chronic mild stress procedure in mice. Pharmacol Biochem Behav 2009, 92:82-87. 10.1016/j.pbb.2008.10.013, 19022280.
39. Wang D, An SC, Zhang X. Prevention of chronic stress-induced depression-like behavior by inducible nitric oxide inhibitor. Neurosci Lett 2008, 433:59-64. 10.1016/j.neulet.2007.12.041, 18248896.
40. Fontella FU, Siqueira IR, Vasconcellos APS, Tabajara AS, Netto CA, Dalmaz C. Repeated restraint stress induces oxidative damage in rat hippocampus. Neurochem Res 2005, 30:105-111. 10.1007/s11064-004-9691-6, 15756938.
41. Lucca G, Comim CM, Valvassori SS, Réus GZ, Vuolo F, Petronilho F, Dal-Pizzol F, Gavioli EC, Quevedo J. Effects of chronic mild stress on the oxidative parameters in the rat brain. Neurochem Int 2009, 54:358-362. 10.1016/j.neuint.2009.01.001, 19171172.
42. Munhoz CD, García-Bueno B, Madriga JL, Lepsch LB, Scavone C, Leza JC. Stress-induced neuroinflammation: mechanisms and new pharmacological targets. Braz J Med Biol Res 2008, 41:1037-1046. 10.1590/S0100-879X2008001200001, 19148364.
43. Smith RS. The macrophage theory of depression. Med Hypotheses 1991, 35:298-306. 10.1016/0306-9877(91)90272-Z, 1943879.
44. Fu X, Zunich SM, O'Connor JC, Kavelaars A, Dantzer R, Kelly KW. Central administration of lipopolysaccharide induces depressive-like behavior in vivo and activates brain indoleamine 2,3 dioxygenase in murine organotypic hippocampal slice cultures. J Neuroinflammation 2010, 7:43-55. 10.1186/1742-2094-7-43, 2921406, 20678226.
45. Spalletta G, Bossù P, Ciaramella A, Bria P, Caltagirone C, Robinson RG. The etiology of poststroke depression: a review of the literature and a new hypothesis involving inflammatory cytokines. Mol Psychiatry 2006, 11:984-991. 10.1038/sj.mp.4001879, 16894392.
46. Goshen I, Kreisel T, Ounallah-Saad H, Renbaum P, Zalzstein Y, Ben-Hur T, Levy-Lahad E, Yirmiya R. A dual role for interleukin-1 in hippocampal-dependent memory processes. Psychoneuroendocrinology 2007, 32:1106-1115. 10.1016/j.psyneuen.2007.09.004, 17976923.
47. Tilleux S, Hermans E. Neuroinflammation and regulation of glial glutamate uptake in neurological disorders. J Neurosci Res 2007, 85:2059-2070. 10.1002/jnr.21325, 17497670.
48. Matute C, Domercq M, Sanchez-Gomez MV. Glutamate-mediated glial injury: mechanisms and clinical importance. Glia 2006, 53:212-224. 10.1002/glia.20275, 16206168.
49. Anisman H, Merali Z, Hayley S. Neurotransmitter, peptide and cytokine processes in relation to depressive disorder: comorbidity between depression and neurodegenerative disorders. Prog Neurobiol 2008, 85:1-74. 10.1016/j.pneurobio.2008.01.004, 18346832.
50. Felger JC, Alagbe O, Hu F, Mook D, Freeman AA, Sanchez MM, Kalin NH, Ratti E, Nemeroff CB, Miller AH. Effects of interferon-alpha on rhesus monkeys: a non-human primate model of cytokine-induced depression. Biol Psychiatry 2007, 62:1324-1333. 10.1016/j.biopsych.2007.05.026, 2149847, 17678633.
51. Hayley S, Poulter MO, Merali Z, Anisman H. The pathogenesis of clinical depression: stressor-and cytokine-induced alterations of neuroplasticity. Neuroscience 2005, 135:659-678. 10.1016/j.neuroscience.2005.03.051, 16154288.
52. Ford DE, Erlinger TP. Depression and C-reactive protein in US adults: data from the Third National Health and Nutrition Examination Survey. Arch Intern Med 2004, 164:1010-1014. 10.1001/archinte.164.9.1010, 15136311.
53. Miller AH, Maletic V, Raison CL. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol Psychiatry 2009, 65:732-741. 10.1016/j.biopsych.2008.11.029, 2680424, 19150053.
54. Miller GE, Chen E, Sze J, Marin T, Arevalo JM, Doll R, Ma R, Cole SW. A functional genomic fingerprint of chronic stress in humans: blunted glucocorticoid and increased NF-kappaB signaling. Biol Psychiatry 2008, 64:266-272. 10.1016/j.biopsych.2008.03.017, 2581622, 18440494.
55. Michael H. Neuroendocrine function and chronic inflammatory stress. Exp Physiol 2002, 87:519-525. 10.1113/eph8702411, 12481925.