Sildenafil provides sustained neuroprotection in the absence of learning recovery following the 4-vessel occlusion/internal carotid artery model of chronic cerebral hypoperfusion in middle-aged rats

Brain Research Bulletin

Volumn 90, Issue 1, 2013, Pages 58-65

  Dias Fiuza Ferreira, Emilene ^a   Valério Romanini, Cássia ^a   Cypriano, Paulo Eduardo ^a   Weffort de Oliveira, Rúbia Maria ^a   Milani, Humberto ^a  

^a Universidade Estadual de Maringa Centro de Ciencias da Saude Faculdade de Medicina   (Brazil)

Author keywords

Brain neurodegeneration; Chronic cerebral hypoperfusion; Learning deficit; Middle aged rat; Neuroprotection; Sildenafil

Indexed keywords

NEUROPROTECTIVE AGENT; SILDENAFIL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASSOCIATION CORTEX; BRAIN PERFUSION; CHRONIC CEREBRAL HYPOPERFUSION; CONTROLLED STUDY; DENTATE GYRUS; DENTATE HILUS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; HISTOPATHOLOGY; INTERNAL CAROTID ARTERY OCCLUSION; LEARNING; LEARNING DISORDER; MALE; MAZE TEST; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; RETROSPLENIAL CORTEX; REWARD; WORKING MEMORY;

ANIMALS; ARTERIAL OCCLUSIVE DISEASES; BRAIN; CAROTID ARTERY, INTERNAL; CELL COUNT; DISEASE MODELS, ANIMAL; LEARNING DISORDERS; MALE; MAZE LEARNING; NEUROPROTECTIVE AGENTS; PIPERAZINES; PURINES; RATS; RATS, WISTAR; REACTION TIME; SULFONES; TIME FACTORS;

EID: 84870538997     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2012.08.010     Document Type: Article

References (37)

1. Arnavaz A., Aurich A., Weissenborn K., Hartmann U., Emrich H.M., Schneider U. Effect of sildenafil (Viagra) on cerebral blood flow velocity: a pilot study. Psychiatry Research 2003, 122:207-209.
2. Aronowski J., Samways E., Strong R., Rhoades H.M., Grotta J.C. An alternative method for the quantitation of neuronal damage after experimental middle cerebral artery occlusion in rats: analysis of behavioral deficits. Journal of Cerebral Blood Flow and Metabolism 1996, 16:705-713.
3. Barros C.A., Ekuni R., Mori M.A., Pereira F.M., Santos Pereira M.A., Milani H. The cognitive and histopathological effects of chronic 4-vessel occlusion in rats depend on the set of vessels occluded and the age of the animals. Behavioural Brain Research 2009, 197:378-387.
4. Caretti P., Bianciardi R., Ronchi R., Fantacci M., Guazzi M., Samaja M. Phosphodiesterase-5 inhibition abolishes neuron apoptosis induced by chronic hypoxia independently of hypoxia-inducible factor-1α signaling. Experimental Biology and Medicine 2008, 233:1222-1230.
5. Colbourne F., Corbett D. Delayed postischemic hypothermia: a six month survival study using behavioral and histological assessments of neuroprotection. Journal of Neuroscience 1995, 15:7250-7260.
6. Corbett D., Crooks P. Ischemic preconditioning: a long term survival study using behavioural and histological endpoints. Brain Research 1997, 760:129-136.
7. Corbett D., Nurse S. The problem of assessing effective neuroprotection in experimental cerebral ischemia. Progress in Neurobiology 1998, 54:531-548.
8. Dalley J.W., Cardinal R.N., Robbins T.W. Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neuroscience and Biobehavioral Reviews 2004, 28:771-784.
9. Das A., Xi L., Kukreja R.C. Phosphodiesterase-5 inhibitor sildenafil preconditions adult cardiac myocytes against necrosis and apoptosis: essential role of nitric oxide signaling. Journal of Biological Chemistry 2005, 280:12944-12955.
10. de la Torre J.C., Kalaria R.N., Nakajima K., Nagata K. Alzheimer's disease: vascular etiology and pathology. Annals of the New York Academy of Sciences, vol. 977 2002, New York, New York Academy of Sciences.
11. de la Torre J.C. Carotid artery ultrasound and echocardiography testing to lower the prevalence of Alzheimer's disease. Journal of Stroke and Cerebrovascular Diseases 2009, 18:319-328.
12. Ding G., et al. Longitudinal magnetic resonance imaging of sildenafil treatment of embolic stroke in aged rats. Stroke 2011, 42:3537-3541.
13. Dirnagl U., Becker K., Meisel A. Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurology 2009, 8:398-412.
14. Eichenbaum H. A cortical-hippocampal system for declarative memory. Nature Reviews Neuroscience 2000, 1:41-50.
15. Ferreira E.D.F., Romanini C.V., Mori M.A., Oliveira R.M.W., Milani H. Middle-aged but not young, rats develop cognitive impairment and cortical neurodegeneration following the four-vessel occlusion/internal carotid artery model of chronic cerebral hypoperfusion. European Journal of Neuroscience 2011, 34:1131-1140.
16. Ghofrani H.A., Osterloh I.H., Grimminger F. Sildenafil: from angina to erectile dysfunction to pulmonary hypertension and beyond. Nature Reviews Drug Discovery 2006, 2006(5):689-702.
17. Green E.J., Dietrich W.D., Van Dijk F., Busto R., Markgraf C.G., McCabe P.M., Ginsberg M.D., Schneiderman N. Protective effects of brain hypothermia on behavior and histopathology following global cerebral ischemia in rats. Brain Research 1992, 580:197-204.
18. Ishimaru H., Takahashi A., Ikarashi Y., Muruyama Y. Pentobarbital protects against CA1 pyramidal cell death but not dysfunction of hippocampal cholinergic neurons following transient ischemia. Brain Research 1995, 673:112-118.
19. Keene C.S., Bucci D.J. Damage to the retrosplenial cortex produces specific impairments in spatial working memory. Neurobiology of Learning and Memory 2009, 91:408-414.
20. Kruuse C., Thomsen L.L., Jacobsen T.B., Olesen J. The phosphodiesterase 5 inhibitor sildenafil has no effect on cerebral blood flow or blood velocity, but nevertheless induces headache in healthy subjects. Journal of Cerebral Blood Flow and Metabolism 2003, 22:1124-1131.
21. Kukreja R.C., et al. Pharmacological preconditioning with sildenafil: basic mechanisms and clinical implications. Vascular Pharmacology 2005, 42:219-232.
22. Lee I., Kesner R.P. Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. Journal of Neuroscience 2003, 23:1517-1523.
23. Li L., et al. Angiogenesis and improved cerebral blood flow in the ischemic boundary area detected by MRI after administration of sildenafil to rats with embolic stroke. Brain Research 2007, 1132:185-192.
24. Menniti F.S., et al. Phosphodiesterase 5A inhibitors improve functional recovery after stroke in rats: optimized dosing regimen with implications for mechanism. Journal of Pharmacology and Experimental Therapeutics 2009, 331:842-850.
25. Neto C.J.B.F., Paganelli R.A., Benetoli A., Lima K.C.M., Milani H. Permanent 3-stage, 4-vessel occlusion as a model of chronic and progressive brain hypoperfusion in rats: a neurohistological and behavioral analysis. Behavioural Brain Research 2005, 160:312-322.
26. Pereira F.M., Ferreira E.D.F., Oliveira R.M.W., Milani H. Time-course of neurodegeneration and memory impairment following the 4-vessel occlusion/internal carotid artery model of chronic cerebral hypoperfusion in middle-aged rats. Behavioural Brain Research 2012, 229:340-348.
27. Prickaerts J., van Staveren W.C.G., Sik A., Markerink-van Ittersum M., Niewöhner U., van der Staay F.J., Blokland A., de Vente J. Effects of two selective phosphodiesterase type 5 inhibitors, sildenafil and vardenafil, on object recognition memory and hippocampal cyclic GMP levels in the rat. Neuroscience 2002, 113:351-361.
28. Prickaerts J., Sik A., van der Staay F.J., de Vente J., Blokland A. Dissociable effects of acetylcholinesterase inhibitors and phosphodiesterase type 5 inhibitors on object recognition memory: acquisition versus consolidation. Psychopharmacology (Berlin) 2005, 177:381-390.
29. Reneerkens O.A., Rutten K., Steinbusch H.W., Blokland A., Prickaerts J. Selective phosphodiesterase inhibitors: a promising target for cognition enhancement. Psychopharmacology (Berlin) 2009, 202:419-443.
30. Romanini C.V., Schiavon A.P., Ferreira E.D.F., Oliveira R.M.W., Milani H. Sildenafil prevents mortality and reduces hippocampal damage after permanent, stepwise, 4-vessel occlusion in rats. Brain Research Bulletin 2010, 81:631-640.
31. Vlachopoulos C., Terentes-Printzios D., Ioakeimidis N., Rokkas K., Stefanadis C. PDE5 inhibitors in non-urological conditions. Current Pharmaceutical Design 2009, 15:3521-3539.
32. Wall P.M., Messier C. The hippocampal formation: orbitomedial prefrontal cortex circuit in the attentional control of active memory. Behavioural Brain Research 2001, 127:99-117.
33. + channels in sildenafil-induced late cardioprotection. Journal of Molecular and Cellular Cardiology 2008, 44:105-113.
34. Watanabe T., Zhang N., Liu M., Tanaka R., Mizuno Y., Urabe T. Cilostazol protects against brain white matter damage and cognitive impairment in a rat model of chronic cerebral hypoperfusion. Stroke 2006, 37:1539-1545.
35. Zhang R., Wang Y., Zhang L., Zhang Z., Tsang W., Lu M., Zhang L., Chopp M. Sildenafil (Viagra) induces neurogenesis and promotes functional recovery after stroke in rats. Stroke 2002, 33:2675-2680.
36. Zhang L., Zhang R.L., Wang Y., Zhang C., Zhang Z.G., Meng H., Chopp M. Functional recovery in aged and young rats after embolic stroke: treatment with a phosphodiesterase type 5 inhibitor. Stroke 2005, 36:847-852.
37. Zhang R.L., Zhang Z., Zhang L., Wang Y., Zhang C., Chopp M. Delayed treatment with sildenafil enhances neurogenesis and improves functional recovery in aged rats after focal cerebral ischemia. Journal of Neuroscience Research 2006, 83:1213-1219.