Protective effects of phosphodiesterase 2 inhibitor on depression- and anxiety-like behaviors: Involvement of antioxidant and anti-apoptotic mechanisms

Behavioural Brain Research

Volumn 268, Issue , 2014, Pages 150-158

  Ding, Lianshu ^a   Zhang, Chong ^b   Masood, Anbrin ^c   Li, Jianxin ^d   Sun, Jiao ^d   Nadeem, Ahmed ^c   Zhang, Han Ting ^c   O'Donnell, James M ^b   Xu, Ying ^b  

^a NANJING MEDICAL UNIVERSITY   (China)

^b UNIVERSITY AT BUFFALO   (United States)

^c WEST VIRGINIA UNIVERSITY   (United States)

^d WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Cyclic GMP; Neuronal apoptosis; Oxidative damage; Phosphodiesterase 2

Indexed keywords

ANTIDEPRESSANT AGENT; ANXIOLYTIC AGENT; BAY 60 7550; CASPASE 3; COPPER ZINC SUPEROXIDE DISMUTASE; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; DESIPRAMINE; DIAZEPAM; PHOSPHODIESTERASE; PHOSPHODIESTERASE 2; PHOSPHODIESTERASE 2 INHIBITOR; PHOSPHODIESTERASE INHIBITOR; PROTEIN BAX; PROTEIN BCL 2; SERINE; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN; 2-(3,4-DIMETHOXYBENZYL)-7-(1-(1-HYDROXYETHYL)-4-PHENYLBUTYL)-5-METHYLIMIDAZO(5,1-F)(1,2,4)TRIAZIN-4 (3H)-ONE; CASP3 PROTEIN, MOUSE; CYCLIC NUCLEOTIDE PHOSPHODIESTERASE 2; IMIDAZOLE DERIVATIVE; PSYCHOTROPIC AGENT; SUPEROXIDE DISMUTASE; TRIAZINE DERIVATIVE;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIAPOPTOTIC ACTIVITY; ANTIOXIDANT ACTIVITY; ANXIETY DISORDER; ARTICLE; BEHAVIOR CHANGE; CHRONIC STRESS; CONTROLLED STUDY; DEPRESSION; DRUG MECHANISM; DRUG MEGADOSE; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME REGULATION; HIPPOCAMPUS; MALE; MENTAL STRESS; MOUSE; NERVE CELL NECROSIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TREATMENT RESPONSE; ANIMAL; ANTAGONISTS AND INHIBITORS; ANXIETY DISORDERS; APOPTOSIS; DEPRESSIVE DISORDER; DRUG EFFECTS; DRUG THERAPY; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY;

AMYGDALA; ANIMALS; ANXIETY DISORDERS; APOPTOSIS; CASPASE 3; CYCLIC GMP; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 2; DEPRESSIVE DISORDER; HIPPOCAMPUS; IMIDAZOLES; MALE; MICE, INBRED ICR; NEURONS; OXIDATIVE STRESS; PHOSPHODIESTERASE INHIBITORS; PSYCHOTROPIC DRUGS; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL; SUPEROXIDE DISMUTASE; TRIAZINES;

EID: 84899576194     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2014.03.042     Document Type: Article

References (56)

1. Kessler R.C., Angermeyer M., Anthony J.C., DE Graaf R., Demyttenaere K., Gasquet I., et al. Lifetime prevalence and age-of-onset distributions of mental disorders in the World Health Organization's World Mental Health Survey Initiative. World Psychiatry 2007, 6:168-176.
2. Madrigal J.L.M., García-Bueno B., Caso J.R., Pérez-Nievas B.G., Leza J.C. Stress-induced oxidative changes in brain. CNS Neurol Disord Drug Targets 2006, 5:561-568.
3. Tell G., Gustincich S. Redox state, oxidative stress, and molecular mechanisms of protective and toxic effects of bilirubin on cells. Curr Pharm Des 2009, 15:2908-2914.
4. Lee W.-Y., Jang S.-W., Lee J.-S., Kim Y.-H., Kim H.-G., Han J.-M., et al. Uwhangchungsimwon, a traditional herbal medicine, protects brain against oxidative injury via modulation of hypothalamus-pituitary-adrenal (HPA) response in a chronic restraint mice model. J Ethnopharmacol 2014, 151:461-469.
5. Kwon D.-H., Kim B.-S., Chang H., Kim Y.-I., Jo S.A., Leem Y.-H. Exercise ameliorates cognition impairment due to restraint stress-induced oxidative insult and reduced BDNF level. Biochem Biophys Res Commun 2013, 434:245-251.
6. McKernan D.P., Dinan T.G., Cryan J.F. "Killing the Blues": a role for cellular suicide (apoptosis) in depression and the antidepressant response?. Prog Neurobiol 2009, 88:246-263.
7. Cory S., Adams J.M. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2002, 2:647-656.
8. Lindsten T., Zong W.-X., Thompson C.B. Defining the role of the Bcl-2 family of proteins in the nervous system. Neuroscientist 2005, 11:10-15.
9. Bravo J.A., Díaz-Veliz G., Mora S., Ulloa J.L., Berthoud V.M., Morales P., et al. Desipramine prevents stress-induced changes in depressive-like behavior and hippocampal markers of neuroprotection. Behav Pharmacol 2009, 20:273-285.
10. Li Y.-F., Cheng Y.-F., Huang Y., Conti M., Wilson S.P., O'Donnell J.M., et al. Phosphodiesterase-4D knock-out and RNA interference-mediated knock-down enhance memory and increase hippocampal neurogenesis via increased cAMP signaling. J Neurosci 2011, 31:172-183.
11. Reneerkens O.A.H., Rutten K., Steinbusch H.W.M., Blokland A., Prickaerts J. Selective phosphodiesterase inhibitors: a promising target for cognition enhancement. Psychopharmacology (Berl) 2009, 202:419-443.
12. Halene T.B., Siegel S.J. PDE inhibitors in psychiatry-future options for dementia, depression and schizophrenia?. Drug Discov Today 2007, 12:870-878.
13. Dlaboga D., Hajjhussein H., O'Donnell J.M. Chronic haloperidol and clozapine produce different patterns of effects on phosphodiesterase-1B, -4B, and -10A expression in rat striatum. Neuropharmacology 2008, 54:745-754.
14. Rundfeldt C., Socała K., Wlaź P. The atypical anxiolytic drug, tofisopam, selectively blocks phosphodiesterase isoenzymes and is active in the mouse model of negative symptoms of psychosis. J Neural Transm 2010, 117:1319-1325.
15. Van Staveren W.C.G., Steinbusch H.W.M., Markerink-Van Ittersum M., Repaske D.R., Goy M.F., Kotera J., et al. mRNA expression patterns of the cGMP-hydrolyzing phosphodiesterases types 2, 5, and 9 during development of the rat brain. J Comp Neurol 2003, 467:566-580.
16. Nikolaev V.O., Gambaryan S., Engelhardt S., Walter U., Lohse M.J. Real-time monitoring of the PDE2 activity of live cells: hormone-stimulated cAMP hydrolysis is faster than hormone-stimulated cAMP synthesis. J Biol Chem 2005, 280:1716-1719.
17. Masood A., Nadeem A., Mustafa S.J., O'Donnell J.M. Reversal of oxidative stress-induced anxiety by inhibition of phosphodiesterase-2 in mice. J Pharmacol Exp Ther 2008, 326:369-379.
18. Xu Y., Pan J., Chen L., Zhang C., Sun J., Li J., et al. Phosphodiesterase-2 inhibitor reverses corticosterone-induced neurotoxicity and related behavioural changes via cGMP/PKG dependent pathway. Int J Neuropsychopharmacol 2013, 16:835-847.
19. Willner P., Muscat R., Papp M. Chronic mild stress-induced anhedonia: a realistic animal model of depression. Neurosci Biobehav Rev 1992, 16:525-534.
20. Ortiz J., Fitzgerald L.W., Lane S., Terwilliger R., Nestler E.J. Biochemical adaptations in the mesolimbic dopamine system in response to repeated stress. Neuropsychopharmacology 1996, 14:443-452.
21. Perrotti L.I., Hadeishi Y., Ulery P.G., Barrot M., Monteggia L., Duman R.S., et al. Induction of deltaFosB in reward-related brain structures after chronic stress. J Neurosci 2004, 24:10594-10602.
22. Steru L., Chermat R., Thierry B., Simon P. The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology (Berl) 1985, 85:367-370.
23. Porsolt R.D., Bertin A., Jalfre M. "Behavioural despair" in rats and mice: strain differences and the effects of imipramine. Eur J Pharmacol 1978, 51:291-294.
24. Masood A., Banerjee B., Vijayan V.K., Ray A. Modulation of stress-induced neurobehavioral changes by nitric oxide in rats. Eur J Pharmacol 2003, 458:135-139.
25. Tsuji M., Takeda H., Matsumiya T. Different effects of 5-HT1A receptor agonists and benzodiazepine anxiolytics on the emotional state of naive and stressed mice: a study using the hole-board test. Psychopharmacology (Berl) 2000, 152:157-166.
26. Skalisz L.L., Beijamini V., Andreatini R. Effect of Hypericum perforatum on marble-burying by mice. Phytother Res 2004, 18:399-402.
27. Dekeyne A., Mannoury la Cour C., Gobert A., Brocco M., Lejeune F., Serres F., et al. S32006, a novel 5-HT2C receptor antagonist displaying broad-based antidepressant and anxiolytic properties in rodent models. Psychopharmacology (Berl) 2008, 199:549-568.
28. Masood A., Huang Y., Hajjhussein H., Xiao L., Li H., Wang W., et al. Anxiolytic effects of phosphodiesterase-2 inhibitors associated with increased cGMP signaling. J Pharmacol Exp Ther 2009, 331:690-699.
29. Alfonso J., Frasch A.C., Flugge G. Chronic stress, depression and antidepressants: effects on gene transcription in the hippocampus. Rev Neurosci 2005, 16:43-56.
30. Xu Y., Ku B., Cui L., Li X., Barish P.a., Foster T.C., et al. Curcumin reverses impaired hippocampal neurogenesis and increases serotonin receptor 1A mRNA and brain-derived neurotrophic factor expression in chronically stressed rats. Brain Res 2007, 1162:9-18.
31. Li Y.-F., Huang Y., Amsdell S.L., Xiao L., O'Donnell J.M., Zhang H.-T. Antidepressant- and anxiolytic-like effects of the phosphodiesterase-4 inhibitor rolipram on behavior depend on cyclic AMP response element binding protein-mediated neurogenesis in the hippocampus. Neuropsychopharmacology 2009, 34:2404-2419.
32. Matsushita H., Matsuzaki M., Han X.-J., Nishiki T.-I., Ohmori I., Michiue H., et al. Antidepressant-like effect of sildenafil through oxytocin-dependent cyclic AMP response element-binding protein phosphorylation. Neuroscience 2012, 200:13-18.
33. Rosman G.J., Martins T.J., Sonnenburg W.K., Beavo J.A., Ferguson K., Loughney K. Isolation and characterization of human cDNAs encoding a cGMP-stimulated 3',5'-cyclic nucleotide phosphodiesterase. Gene 1997, 191:89-95.
34. Peluffo H., Acarin L., Faiz M., Castellano B., Gonzalez B. Cu/Zn superoxide dismutase expression in the postnatal rat brain following an excitotoxic injury. J Neuroinflammation 2005, 2:12.
35. McIntosh L.J., Hong K.E., Sapolsky R.M. Glucocorticoids may alter antioxidant enzyme capacity in the brain: baseline studies. Brain Res 1998, 791:209-214.
36. Grundmann O, Lv Y, Kelber O, Butterweck V. Mechanism of St. John's wort extract (STW3-VI) during chronic restraint stress is mediated by the interrelationship of the immune, oxidative defense, and neuroendocrine system. Neuropharmacology n.d.;58:767-73.
37. Lucca G, Comim CM, Valvassori SS, Réus GZ, Vuolo F, Petronilho F, et al. Effects of chronic mild stress on the oxidative parameters in the rat brain. Neurochem Int n.d.;54:358-62.
38. Liu W., Zhou C. Corticosterone reduces brain mitochondrial function and expression of mitofusin, BDNF in depression-like rodents regardless of exercise preconditioning. Psychoneuroendocrinology 2012, 37:1057-1070.
39. Kirby E.D., Friedman A.R., Covarrubias D., Ying C., Sun W.G., Goosens K.A., et al. Basolateral amygdala regulation of adult hippocampal neurogenesis and fear-related activation of newborn neurons. Mol Psychiatry 2012, 17:527-536.
40. Whittle N., Li L., Chen W.-Q., Yang J.-W., Sartori S.B., Lubec G., et al. Changes in brain protein expression are linked to magnesium restriction-induced depression-like behavior. Amino Acids 2011, 40:1231-1248.
41. Tanti A., Belzung C. Open questions in current models of antidepressant action. Br J Pharmacol 2010, 159:1187-1200.
42. Nakamizo T., Kawamata J., Yoshida K., Kawai Y., Kanki R., Sawada H., et al. Phosphodiesterase inhibitors are neuroprotective to cultured spinal motor neurons. J Neurosci Res 2003, 71:485-495.
43. Pifarré P., Prado J., Giralt M., Molinero A., Hidalgo J., Garcia A. Cyclic GMP phosphodiesterase inhibition alters the glial inflammatory response, reduces oxidative stress and cell death and increases angiogenesis following focal brain injury. J Neurochem 2010, 112:807-817.
44. Mattson M.P., Guo Z.H., Geiger J.D. Secreted form of amyloid precursor protein enhances basal glucose and glutamate transport and protects against oxidative impairment of glucose and glutamate transport in synaptosomes by a cyclic GMP-mediated mechanism. J Neurochem 1999, 73:532-537.
45. Urushitani M., Inoue R., Nakamizo T., Sawada H., Shibasaki H., Shimohama S. Neuroprotective effect of cyclic GMP against radical-induced toxicity in cultured spinal motor neurons. J Neurosci Res 2000, 61:443-448.
46. Boess F.G., Hendrix M., van der Staay F.-J., Erb C., Schreiber R., van Staveren W., et al. Inhibition of phosphodiesterase 2 increases neuronal cGMP, synaptic plasticity and memory performance. Neuropharmacology 2004, 47:1081-1092.
47. Jiménez-Velázquez G., López-Muñoz F.J., Fernández-Guasti A. Participation of the GABA/benzodiazepine receptor and the NO-cyclicGMP pathway in the "antinociceptive-like effects" of diazepam. Pharmacol Biochem Behav 2008, 91:128-133.
48. Gaur V., Kumar A. Protective effect of desipramine, venlafaxine and trazodone against experimental animal model of transient global ischemia: possible involvement of NO-cGMP pathway. Brain Res 2010, 1353:204-212.
49. Aquilano K., Baldelli S., Cardaci S., Rotilio G., Ciriolo M.R. Nitric oxide is the primary mediator of cytotoxicity induced by GSH depletion in neuronal cells. J Cell Sci 2011, 124:1043-1054.
50. Polster B.M., Fiskum G. Mitochondrial mechanisms of neural cell apoptosis. J Neurochem 2004, 90:1281-1289.
51. Agrawal M., Kumar V., Kashyap M.P., Khanna V.K., Randhawa G.S., Pant A.B. Ischemic insult induced apoptotic changes in PC12 cells: protection by trans resveratrol. Eur J Pharmacol 2011, 666:5-11.
52. Chen D.F., Schneider G.E., Martinou J.C., Tonegawa S. Bcl-2 promotes regeneration of severed axons in mammalian CNS. Nature 1997, 385:434-439.
53. Kaufmann J.A., Bickford P.C., Taglialatela G. Oxidative-stress-dependent up-regulation of Bcl-2 expression in the central nervous system of aged Fisher-344 rats. J Neurochem 2001, 76:1099-1108.
54. Djordjevic A., Djordjevic J., Elaković I., Adzic M., Matić G., Radojcic M.B. Fluoxetine affects hippocampal plasticity, apoptosis and depressive-like behavior of chronically isolated rats. Prog Neuropsychopharmacol Biol Psychiatry 2012, 36:92-100.
55. Sharma D.R., Sunkaria A., Bal A., Bhutia Y.D., Vijayaraghavan R., Flora S.J.S., et al. Neurobehavioral impairments, generation of oxidative stress and release of pro-apoptotic factors after chronic exposure to sulphur mustard in mouse brain. Toxicol Appl Pharmacol 2009, 240:208-218.
56. Park J.R., Hockenbery D.M. BCL-2, a novel regulator of apoptosis. J Cell Biochem 1996, 60:12-17.