Inhibition of phosphodiesterase 2 reverses impaired cognition and neuronal remodeling caused by chronic stress

Neurobiology of Aging

Volumn 36, Issue 2, 2015, Pages 955-970

  Xu, Ying ^a,b   Pan, Jianchun ^a   Sun, Jiao ^a   Ding, Lianshu ^c   Ruan, Lina ^a   Reed, Miranda ^d   Yu, Xuefeng ^a   klabnik, Jonathan ^d   Lin, Dan ^a   Li, Jianxin ^a   Chen, Ling ^a   Zhang, Chong ^b   Zhang, Hanting ^d   O'Donnell, James M ^b  

^a WENZHOU MEDICAL UNIVERSITY   (China)

^b UNIVERSITY AT BUFFALO   (United States)

^c NANJING MEDICAL UNIVERSITY   (China)

^d WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

Bay 60 7550; Cognition; Neuroplasticity; PDE2; Stress

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CYCLIC AMP; CYCLIC GMP; EARLY GROWTH RESPONSE FACTOR 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHOSPHODIESTERASE INHIBITOR; SPLEEN EXONUCLEASE; UNCLASSIFIED DRUG; [2 [(3,4 DIMETHOXYPHENYL)METHYL] 7 [1 HYDROXYETHYL] 4 PHENYLBUTYL] 5 METHYL IMIDAZO[5,1 F][1,2,4]TRIAZIN 4(1H) ONE; 2-(3,4-DIMETHOXYBENZYL)-7-(1-(1-HYDROXYETHYL)-4-PHENYLBUTYL)-5-METHYLIMIDAZO(5,1-F)(1,2,4)TRIAZIN-4 (3H)-ONE; CYCLIC NUCLEOTIDE PHOSPHODIESTERASE 2; IMIDAZOLE DERIVATIVE; TRIAZINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CHRONIC STRESS; COGNITIVE DEFECT; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME INHIBITION; HIPPOCAMPAL CA1 REGION; MALE; MEMORY DISORDER; MORRIS WATER MAZE TEST; MOUSE; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; SIGNAL TRANSDUCTION; SPATIAL LEARNING; SPATIAL MEMORY; ANIMAL; ANTAGONISTS AND INHIBITORS; CHRONIC DISEASE; COGNITION; COGNITION DISORDERS; CYTOLOGY; DRUG EFFECTS; GENETICS; HIPPOCAMPUS; INSTITUTE FOR CANCER RESEARCH MOUSE; MENTAL STRESS; NERVE CELL; NERVE REGENERATION; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY;

ANIMALS; CHRONIC DISEASE; COGNITION; COGNITION DISORDERS; CYCLIC AMP; CYCLIC GMP; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 2; HIPPOCAMPUS; IMIDAZOLES; MALE; MICE, INBRED ICR; NERVE REGENERATION; NEURONAL PLASTICITY; NEURONS; PHOSPHODIESTERASE INHIBITORS; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL; TRIAZINES;

EID: 84922772288     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.08.028     Document Type: Article

References (60)

1. Azzouni F., Abu samra K. Are phosphodiesterase type 5 inhibitors associated with vision-threatening adverse events? A critical analysis and review of the literature. J.Sex Med. 2011, 8:2894-2903.
2. Birnbaum S.G., Yuan P.X., Wang M., Vijayraghavan S., Bloom A.K., Davis D.J., Gobeske K.T., Sweatt J.D., Manji H.K., Arnsten A.F. Protein kinase C overactivity impairs prefrontal cortical regulation of working memory. Science 2004, 306:882-884.
3. Blokland A., Schreiber R., Prickaerts J. Improving memory: a role for phosphodiesterases. Curr. Pharm. 2006, 12:2511-2523.
4. Bodhinathan K., Kumar A., Foster T.C. Redox sensitive calcium stores underlie enhanced after hyperpolarization of aged neurons: role for ryanodine receptor mediated calcium signaling. J.Neurophysiol. 2010, 104:2586-2593.
5. Bollen E., Puzzo D., Rutten K., Privitera L., De Vry J., Vanmierio T., Kenis G., Palmeri A., D'Hooge R., Balschun D., Steinbusch H.M., Blokland A., Prickaerts J. Improved long-term memory via enhancing cGMP-PKG signaling requires cAMP-PKA signaling. Neuropsychopharmacology 2014, in press.
6. Burns F., Zhao A., Beavo J.A. Cyclic nucleotide phosphodiesterases: gene complexity, regulation by phosphorylation and physiological implications. Adv. Pharmacol. 1996, 36:39-48.
7. Chen J., Wooddruff M.L., Wang T., Concepcion F.A., Tranchina D., Fain G.L. Channel modulation and the mechanism of light adaptation in mouse rods. J Neurosic 2010, 30:16232-16240.
8. Cho T., Ryu J.K., Taghibiglou C., Ge Y., Chan A.W., Liu L., Lu J., McLarnon J.G., Wang Y.T. Long-term potentiation promotes proliferation/survival and neuronal differentiation of neural stem/progenitor cells. PLoS One 2013, 8:e76860.
9. Clayton N.S., Griffiths D.P., Emery N.J., Dickinson A. Elements of episodic-like memory in animals. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2001, 356:1483-1491.
10. De Lima M.N., Laranja D.C., Bromberg E., Roesler R., Schroder N. Pre- or post-training administration of the NMDA receptor blocker MK-801 impairs object recognition memory in rats. Behav. Brain Res. 2005, 156:139-143.
11. Dere E., Huston J.P., De Souza Silva M.A. Integrated memory for objects, places, and temporal order: evidence for episodic-like memory in mice. Neurobiol. Learn Mem. 2005, 84:214-221.
12. Deshmukh R., Sharma V., Mehan S., Sharma N., Bedi K.L. Amelioration of intracerebroventricular streptozotocin induced cognitive dysfunction and oxidative stress by vinpocetine-a PDE1 inhibitor. Eur. J. Pharmacol. 2009, 620:49-56.
13. Ennaceur A., Neave N., Aggleton J.P. Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp. Brain Res. 1997, 113:509-519.
14. Finkbeiner S., Tavazoie S.F., Maloratsky A., Jacobs K.M., Harris K.M., Greenberg M.E. CREB: a major mediator of neuronal neurotrophin responses. Neuron 1997, 19:1031-1047.
15. Flavell S.W., Greenberg M.E. Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu. Rev. Neurosci. 2008, 31:563-590.
16. Franklin K.B.J., Paxinos G. The Mouse Brain in Stereotaxic Coordinates 1997, Academic Press, San Diego.
17. Gallo E.F., Iadecola C. Neuronal nitric oxide contributes to neuroplasticity-associated protein expression through cGMP, protein kinase G, and extracellular signal-regulated kinase. J.Neurosci. 2011, 31:6947-6955.
18. García-Osta A., Cuadrado-Tejedor M., García-Barroso C., Oyarzábal J., Franco R. Phosphodiesterases as therapeutic targets for Alzheimer's disease. ACS Chem. Neurosci. 2012, 3:832-844.
19. Gille H., Strahl T., Shaw P.E. Activation of ternary complex factor Elk-1 by stress-activated protein kinases. Curr. Biol. 1995, 5:1191-1200.
20. Girotti M., Weinberg M.S., Spencer R.L. Differential responses of hypothalamus-pituitary-adrenal axis immediate early genes to corticosterone and circadian drive. Endocrinology 2007, 148:2542-2552.
21. Gourley S.L., Swanson A.M., Koleske A.J. Corticosteroid-induced neural remodeling predicts behavioral vulnerability and resilience. J.Neurosci. 2013, 33:3107-3112.
22. Hains A.B., Vu M.A.T., Maciejewski P.K., van Dyck C.H., Gottron M., Arnsten A.F. Inhibition of protein kinase C signaling protects prefrontal cortex dendritic spines and cognition from the effects of chronic stress. Proc. Natl. Acad. Sci. U.S.A 2009, 106:17957-17962.
23. Huang Y.Y., Li X.C., Kandel E.R. cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell 1994, 79:69-79.
24. Impey S., Mark M., Villacres E.C., Poser S., Chavkin C., Storm D.R. Induction of CRE-mediated gene expression by stimuli that generate long-lasting LTP in area CA1 of the hippocampus. Neuron 1996, 16:973-982.
25. Idigo W.O., Reilly S., Zhang M.H., Zhang Y.H., Jayaram R., Carnicer R., Crabtree M.J., Balligand J.L., Casadei B. Regulation of endothelial nitric-oxide synthase (NOS) s-glutathionylation by neuronal NOS: evidence of a functional interaction between myocardial constitutive NOS isoforms. J.Biol. Chem. 2012, 287:43665-43673.
26. Kleppisch T. Phosphodiesterases in the central nervous system. Handb Exp. Pharmacol. 2009, 191:71-92.
27. Lee H.Y., Yang B.C., Lee E.S., Chung J.I., Koh P.O., Park M.S., Kim M.O. Modulation by the GABA (B) receptor siRNA of ethanol-mediated PKA-α, CaMKII, and p-CREB intracellular signaling in prenatal rat hippocampal neurons. Anat. Cell Biol. 2011, 44:210-217.
28. Li Y.F., Cheng Y.F., Huang Y., Conti M., Wilson S.P., O'Donnell J.M., Zhang H.T. 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.
29. Lu Y.F., Kandel E.R., Hawkins R.D. Nitric oxide signaling contributes to late-phase LTP and CREB phosphorylation in the hippocampus. J.Neurosci. 1999, 19:10250-10261.
30. Martinez-Finley E.J., Goggin S.L., Labrecque M.T., Allan A.M. Reduced expression of MAPK/ERK genes in perinatal arsenic-exposed offspring induced by glucocorticoid receptor deficits. Neurotoxicol. Teratol. 2011, 33:530-537.
31. McEwen B.S. Effects of adverse experiences for brain structure and function. Biol. Psychiatry 2000, 48:721-731.
32. McLaughlin K.J., Gomez J.L., Baran S.E., Conrad C.D. The effects of chronic stress on hippocampal morphology and function: an evaluation of chronic restraint paradigms. Brain Res. 2007, 1161:56-64.
33. Mitra R., Sapolsky R.M. Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy. Proc. Natl. Acad. Sci. U.S.A 2008, 105:5573-5578.
34. Morris R.G. Episodic-like memory in animals: psychological criteria, neural mechanisms and the value of episodic-like tasks to investigate animal models of neurodegenerative disease. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2001, 356:1453-1465.
35. Nicholas A., Munhoz C.D., Ferguson D., Campbell L., Sapolsky R. Enhancing cognition after stress with gene therapy. J.Neurosci. 2006, 26:11637-11643.
36. Ortega F., Pérez-Sen R., Delicado E.G., Teresa Miras-Portugal M. ERK1/2 activation is involved in the neuroprotective action of P2Y13 and P2X7 receptors against glutamate excitotoxicity in cerebellar granule neurons. Neuropharmacology 2011, 61:1210-1221.
37. 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.
38. Palumbo M.L., Fosser N.S., Rios H., Zorrilla Zubilete M.A., Guelman L.R., Cremaschi G.A., Genaro A.M. Loss of hippocampal neuronal nitric oxide synthase contributes to the stress-related deficit in learning and memory. J.Neurochem. 2007, 102:261-274.
39. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2005, Elsevier Academic Press, California.
40. Perrotti L.I., Hadeishi Y., Ulery P.G., Barrot M., Monteggia L., Duman R.S., Nestler E.J. Induction of deltaFosB in reward-related brain structures after chronic stress. J.Neurosci. 2004, 24:10594-10602.
41. Reddy P.H., Mani G., Park B.S., Jacques J., Murdoch G., Whetsell W.J., Kaye J., Manczak M. Differential loss of synaptic proteins in Alzheimer's disease: implications for synaptic dysfunction. J.Alzheimers Dis. 2005, 7:103-117.
42. Reneerkens O.A.H., Rutten K., Bollen E., Hage T., Blokland A., Steinbusch H.W.M., Prickaerts J. Inhibition of phosphodiesterase type 2 or type 10 reverses object memory deficits induced by scopolamine or MK-801. Behav. Brain Res. 2013, 236:16-22.
43. Reneerkens O.A.H., Rutten K., Steinbusch H.W.M., Blokland A., Prickaerts J. Selective phosphodiesterase inhibitors: a promising target for cognition enhancement. Psychoppharmacology 2009, 202:419-443.
44. Robichaud A., Savoie C., Stamatiou P.B., Lachance N., Jolicoeur P., Rasori R., Chan C.C. Assessing the emetic potential of PDE4 inhibitors in rats. Br. J. Pharmacol. 2002, 135:113-118.
45. Rodefer J.S., Saland S.K., Eckrich S.J. Selective phosphodiesterase inhibitors improve performance on the ED/ID cognitive task in rats. Neuropharmacology 2012, 62:1182-1190.
46. Rutten K., Van Donkelaar E.L., Ferrington L., Blokland A., Bollen E., Steinbusch H.W.M., Kelly P.A.T., Prickaerts H.H.J. Phosphodiesterase inhibitors enhance object memory independent of cerebral bloodflow and glucose utilization in rats. Neuropsychopharmacology 2009, 34:1914-1925.
47. Shankaranarayana Rao B.S., Govindaiah Laxmi T.R., Meti B.L., Raju T.R. Subicular lesions cause dendritic atrophy in CA1 and CA3 pyramidal neurons of the rat hippocampus. Neuroscience 2001, 102:319-327.
48. Sierksma A.S., Rutten K., Sydlik S., Rostamian S., Steinbusch H.W., van den Hove D.L., Prickaerts J. Chronic phosphodiesterase type 2 inhibition improves memory in the APPswe/PS1dE9 mouse model of Alzheimer's disease. Neuropharmacology 2013, 64:124-136.
49. Suvarna N., O'Donnell J.M. Hydrolysis of N-Methyl-D-aspartate receptor-stimulated cAMP and cGMP by PDE4 and PDE2 phosphodiesterases in primary neuronal cultures of rat cerebral cortex and hippocampus. J.Pharmacol. Exp. Ther. 2002, 302:249-256.
50. Thomas G.M., Huganir R.L. MAPK cascade signaling and synaptic plasticity. Nat. Rev. Neurosci. 2004, 5:173-183.
51. Titus A.D.J., Rao B.S.S., Harsha H.N., Ramkumar K., Srikuma B.N., Singh S.B., Charrarji S., Raju T.R. Hypobaric hypoxia-induced dendritic atrophy of hippocampal neurons is associated with cognitive impairment in adult rats. Neuroscience 2007, 145:265-278.
52. van Donkelaar E.L., Rutten K., Blokland A., Akkerman S., Steinbusch H.W.M., Prickaerts J. Phosphodiesterase 2 and 5 inhibition attenuates the object memory deficit induced by acute tryptophan depletion. Eur. J. Pharmacol. 2008, 600:98-104.
53. Van Staveren W.C., Steinbusch H.W., Markerink-Van Ittersum M., Repaske D.R., Goy M.F., Kotera J., Omori K., Beavo J.A., de Vente J. mRNA expression patterns of the cGMP-hydrolyzing phosphodiesterases types 2, 5, and 9 during development of the rat brain. J.Comp. Neurol. 2003, 888:275-286.
54. Vyas A., Mitra R., Shankaranarayana Rao B.S., Chattarji S. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 2002, 22:6810-6818.
55. Willner P., Muscat R., Papp M. Chronic mild stress-induced anhedonia: a realistic animal model of depression. Neurosci. Biobehav Rev. 1992, 16:525-534.
56. Wisden W., Errington M.L., Williams S., Dunnett S.B., Waters C., Hitchcock D., Evan G., Bliss T.V., Hunt S.P. Differential expression of immediate early genes in the hippocampus and spinal cord. Neuron 1990, 4:603-614.
57. Xu Y., Lin D., Li S., Li G.W., Shyamala S.G., Barish P.A., Vernon M.M., Pan J.C., Ogle W.O. Curcumin reverses impaired cognition and neuronal plasticity induced by chronic stress. Neuropharmacology 2009, 57:463-471.
58. Xu Y., Pan J., Chen L., Zhang C., Sun J., Li J., Nguyen L., Nair N., Zhang H., O'Donnell J.M. Phosphodiesterase-2 inhibitor reverses corticosterone-induced neurotoxicity and related behavioural changes via cGMP/PKG dependent pathway. Int. J. Neuropsychopharmacol. 2013, 16:835-847.
59. Xu Y., Zhang H.T., O'Donnell J.M. Phosphodiesterases in the central nervous system: implications in mood and cognitive disorders. Handb Exp. Pharmacol. 2011, 204:447-485.
60. Zhang H.T., Huang Y., Suvarna N.U., Deng C., Crissman A.M., Hopper A.T., De Vivo M., Rose G.M., O'Donnell J.M. Effects of the novel PDE4 inhibitors MEM1018 and MEM1091 on memory in the radial-arm maze and inhibitory avoidance tests in rats. Psychopharmacology 2005, 179:613-619.