A critical role of NO/cGMP/PKG dependent pathway in hippocampal post-ischemic LTP: Modulation by zonisamide

Neurobiology of Disease

Volumn 44, Issue 2, 2011, Pages 185-191

  Costa, Cinzia ^a,b   Tozzi, Alessandro ^a,b   Siliquini, Sabrina ^a,b   Galletti, Francesca ^a,b   Cardaioli, Gabriela ^a,b   Tantucci, Michela ^a,b   Pisani, Francesco ^c   Calabresi, Paolo ^a,b  

^a UNIVERSITY OF PERUGIA   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c UNIVERSITY OF MESSINA   (Italy)

Author keywords

Antiepileptic drugs; Brain ischemia; Excitatory synaptic transmission; Long term potentiation; Neuroprotection; Nitric oxide; Stroke

Indexed keywords

CYCLIC GMP; GLUCOSE; GUANYLATE CYCLASE INHIBITOR; NITRIC OXIDE; NITRIC OXIDE DONOR; NITRIC OXIDE SYNTHASE INHIBITOR; OXYGEN; ZAPRINAST; ZONISAMIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CONTROLLED STUDY; HIPPOCAMPAL CA1 REGION; LEARNING; LONG TERM POTENTIATION; MALE; MEMORY; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

ANIMALS; ANTICONVULSANTS; BRAIN ISCHEMIA; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; ISOXAZOLES; LONG-TERM POTENTIATION; MALE; NEUROPROTECTIVE AGENTS; NITRIC OXIDE; ORGAN CULTURE TECHNIQUES; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION;

EID: 80052285368     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.06.015     Document Type: Article

References (40)

1. Arancio O., Kiebler M., Lee C.J., Lev-Ram V., Tsien R.Y., Kandel E.R., Hawkins R.D. Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons. Cell 1996, 87:1025-1035.
2. Biton V. Clinical pharmacology and mechanism of action of zonisamide. Clin. Neuropharmacol. 2007, 30:230-240.
3. Bohme G.A., Bon C., Stutzmann J.M., Doble A., Blanchard J.C. Possible involvement of nitric oxide in long-term potentiation. Eur. J. Pharmacol. 1991, 199:379-381.
4. Boulton C.L., Southam E., Garthwaite J. Nitric oxide-dependent long-term potentiation is blocked by a specific inhibitor of soluble guanylyl cyclase. Neuroscience 1995, 69:699-703.
5. Burette A., Zabel U., Weinberg R.J., Schmidt H.H.H.W., Valtschanoff J.G. Synaptic localization of nitric oxide synthase and soluble guanylyl cyclase in the hippocampus. J. Neurosci. 2002, 22:8961-8970.
6. Calabrese V., Bates T.E., Stella A.M. NO synthase and NO-dependent signal pathways in brain aging and neurodegenerative disorders: the role of oxidant/antioxidant balance. Neurochem. Res. 2000, 25:1315-1341.
7. 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.
8. Calabresi P., Centonze D., Pisani A., Cupini L., Bernardi G. Synaptic plasticity in the ischaemic brain. Lancet Neurol. 2003, 2:622-629.
9. Calabresi P., Cupini L.M., Centonze D., Pisani F., Bernardi G. Antiepileptic drugs as a possible neuroprotective strategy in brain ischemia. Ann. Neurol. 2003, 53:693-702.
10. Costa C., Leone G., Saulle E., Pisani F., Bernardi G., Calabresi P. Coactivation of GABA(A) and GABA(B) receptor results in neuroprotection during in vitro ischemia. Stroke 2004, 35:596-600.
11. Costa C., Martella G., Picconi B., Prosperetti C., Pisani A., Di Filippo M., Pisani F., Bernardi G., Calabresi P. Multiple mechanisms underlying the neuroprotective effects of antiepileptic drugs against in vitro ischemia. Stroke 2006, 37:1319-1326.
12. Costa C., Belcastro V., Tozzi A., Di Filippo M., Tantucci M., Siliquini S., Autuori A., Picconi B., Spillantini M.G., Fedele E., Pittaluga A., Raiteri M., Calabresi P. Electrophysiology and pharmacology of striatal neuronal dysfunction induced by mitochondrial complex I inhibition. J. Neurosci. 2008, 28:8040-8052.
13. Costa C., Tozzi A., Luchetti E., Siliquini S., Belcastro V., Tantucci M., Picconi B., Ientile R., Calabresi P., Pisani F. Electrophysiological actions of zonisamide on striatal neurons: selective neuroprotection against complex I mitochondrial dysfunction. Exp. Neurol. 2010, 221:217-224.
14. Crepel V., Ben-Ari Y. Intracellular injection of a Ca2+ chelator prevents generation of anoxic LTP. J. Neurophysiol. 1996, 75:770-779.
15. Crepel V., Hammond C., Chinestra P., Diabira D., Ben-Ari Y. A selective LTP of NMDA receptor-mediated currents induced by anoxia in CA1 hippocampal neurons. J. Neurophysiol. 1993, 70:2045-2055.
16. Crepel V., Epsztein J., Ben-Ari Y. Ischemia induces short- and long-term remodeling of synaptic activity in the hippocampus. J. Cell. Mol. Med. 2003, 7:401-407.
17. Di Filippo M., Tozzi A., Costa C., Belcastro V., Tantucci M., Picconi B., Calabresi P. Plasticity and repair in the post-ischemic brain. Neuropharmacology 2008, 55:353-362.
18. Dirnagl U., Iadecola C., Moskowitz M.A. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 1999, 22:391-397.
19. Fedele E., Raiteri M. In vivo studies of the cerebral glutamate receptor/NO/cGMP pathway. Prog. Neurobiol. 1999, 58:89-120.
20. Garthwaite J., Southam E., Boulton C.L., Nielsen E.B., Schmidt K., Mayer B. Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. Mol. Pharmacol. 1995, 48:184-188.
21. Hayakawa T., Higuchi Y., Nigami H., Hattori H. Zonisamide reduces hypoxic-ischemic brain damage in neonatal rats irrespective of its anticonvulsive effect. Eur. J. Pharmacol. 1994, 257:131-136.
22. Holscher C. Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity. Trends Neurosci. 1997, 20:298-303.
23. Hopper R.A., Garthwaite J. Tonic and phasic nitric oxide signals in hippocampal long-term potentiation. J. Neurosci. 2006, 26:11513-11521.
24. Hsu K.S., Huang C.C. Characterization of the anoxia-induced long-term synaptic potentiation in area CA1 of the rat hippocampus. British J. Pharmacol. 1997, 122:671-681.
25. Hsu K.S., Huang C.C. Protein kinase C inhibitors block generation of anoxia-induced long-term potentiation. Neuroreport 1998, 9:3525-3529.
26. Huang C.C., Hsu K.S. Nitric oxide signalling is required for the generation of anoxia-induced long-term potentiation in the hippocampus. Eur. J. Neurosci. 1997, 9:2202-2206.
27. Iadecola C. Bright and dark sides of nitric oxide in ischemic brain injury. Trends Neurosci. 1997, 20:132-139.
28. Malenka R.C., Nicoll R.A. Long-term potentiation: a decade of progress?. Science 1999, 285:1870-1874.
29. Minato H., Kikuta C., Fujitani B., Masuda Y. Protective effect of zonisamide, an antiepileptic drug, against transient focal cerebral ischemia with middle cerebral artery occlusion-reperfusion in rats. Epilepsia 1997, 38:975-980.
30. Moore P.K., Handy R.L. Selective inhibitors of neuronal nitric oxide synthase: is no NOS really good NOS for the nervous system?. Trends Pharmacol. Sci. 1997, 18:204-211.
31. Noda Y., Mori A., Packer L. Zonisamide inhibits nitric oxide synthase activity induced by N-methyl-D-aspartate and buthionine sulfoximine in the rat hippocampus. Res. Commun. Mol. Pathol. Pharmacol. 1999, 105:23-33.
32. O'Dell T.J., Hawkins R.D., Kandel E.R., Arancio O. Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:11285-11289.
33. Owen A.J., Ijaz S., Miyashita H., Wishart T., Howlett W., Shuaib A. Zonisamide as a neuroprotective agent in an adult gerbil model of global forebrain ischemia: a histological, in vivo microdialysis and behavioral study. Brain Res. 1997, 770:115-122.
34. Phillips K.G., Hardingham N.R., Fox K. Postsynaptic action potentials are required for nitric-oxide-dependent long-term potentiation in CA1 neurons of adult GluR1 knock-out and wild-type mice. J. Neurosci. 2008, 28:14031-14041.
35. Picconi B., Tortiglione A., Barone I., Centonze D., Gardoni F., Gubellini P., Bonsi P., Pisani A., Bernardi G., Di Luca M., Calabresi P. NR2B subunit exerts a critical role in postischemic synaptic plasticity. Stroke 2006, 37:1895-1901.
36. Rosler T.W., Arias-Carrion O., Hoglinger G.U. Zonisamide: aspects in neuroprotection. Exp. Neurol. 2010, 224:336-339.
37. Schuman E.M., Madison D.V. A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 1991, 254:1503-1506.
38. Tozzi A., Costa C., Di Filippo M., Tantucci M., Siliquini S., Belcastro V., Parnetti L., Picconi B., Calabresi P. Memantine reduces neuronal dysfunctions triggered by in vitro ischemia and 3-nitropropionic acid. Exp. Neurol. 2007, 207:218-226.
39. Ueda Y., Doi T., Tokumaru J., Nakajima A., Nagatomo K. In vivo evaluation of the effect of zonisamide on the hippocampal redox state during kainic acid-induced seizure status in rats. Neurochem. Res. 2005, 30:1117-1121.
40. Wendland B., Schweizer F.E., Ryan T.A., Nakane M., Murad F., Sheller R.H., Tsien R.W. Existence of nitric oxide synthase in rat hippocampal pyramidal cells. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:2151-2155.