Nitric oxide and brain hyperexcitability

In Vivo

Volumn 18, Issue 3, 2004, Pages 357-366

  Ferraro, Giuseppe ^a   Sardo, Pierangelo ^a  

^a UNIVERSITY OF PALERMO   (Italy)

Author keywords

Epilepsy; GABA; Glutamate; Nitric oxide; Review

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER; NITRIC OXIDE;

BRAIN NERVE CELL; CELL COMMUNICATION; CELL FUNCTION; EPILEPSY; NERVE CELL EXCITABILITY; NONHUMAN; REVIEW;

EID: 4043124791     PISSN: 0258851X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (96)

1. Snyder SH: Nitric oxide and neurones. Curr Op Neurobiol 2: 323-327, 1992.
2. Palmer RMJ, Ferrige AG and Moncada S: Nitric oxide release accounts for the biological activity of endothelium-derived relaxation factor. Nature 327: 524-526, 1987.
3. Vizi ES: Non Synaptic Interactions Between Neurones: Modulation of Neurochemical Transmission. John Wiley and Sons, 1984.
4. Vizi ES: Role of high-affinity receptors and membrane transporters in non synaptic communication and drug action in the central nervous system. Pharmacol Rev 52: 63-90, 2000.
5. Bredt DS, Glatt CE, Hwang PM, Fotuhi M, Dawson TM and Snyder SH: Nitric oxide synthase protein and mRNA are discretely localised in neuronal populations of mammalian central nervous system together with NADPH diaphorase. Neuron 7: 615-624, 1991.
6. Lowenstein CJ, Glatt CS, Bredt DS and Snyder SH: Cloned and expressed macrophage nitric oxide synthase contrasts with the brain enzyme. Proc Natl Acad Sci USA 89: 6711-6715, 1992.
7. Sessa WC, Harrison JK, Barber CM, Zeng D, Durieux MS, D'Angelo DD, Lynch KR and Peach MJ: Molecular cloning and expression of a cDNA encoding endothelial cell nitric oxide synthase. J Biol Chem 267: 15274-15276, 1992.
8. Bredt DS and Snyder SH: Nitric oxide: a physiological messenger molecule. Ann Rev Biochem 63: 175-179, 1994.
9. 2+/calmodulin-regulated nitric oxide synthase. Cell Calcium 13: 427-434, 1992.
10. Dinerman JL, Dawson TM, Schell MJ, Snowman A and Snyder SH: Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: implications for synaptic plasticity. Proc Natl Acad Sci USA 91: 4214-4218, 1994.
11. Garthwaite J and Boulton CL: Nitric oxide signalling in the central nervous system. Ann Rev Physiol 57: 683-706, 1995.
12. Luo D, Das S and Vincent SR: Effects of methylene blue and LY83583 on neuronal nitric oxide synthase and NADPH-diaphorase. Eur J Pharmacol 290: 247-251, 1995.
13. Dawson VL and Dawson TM: Nitric oxide in neurodegeneration. Progr Brain Res 118: 215-229, 1998.
14. Ahern GP, Klyachko VA and Jackson MB: cGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO. Trends Neurosci 25: 510-517, 2002.
15. de Vente J, Hopkins DA, Markerink-Van Ittersum M, Emson PC, Schmidt HHHW and Steinbusch HWM: Distribution of nitric oxide synthase and nitric oxide-receptive, cyclic GMP-producing structures in the rat brain. Neuroscience 87: 207-241, 1998.
16. Iwase K, Iyama K, Akagi K, Yano S, Fukunaga K, Miyamoto E, Mori M and Takiguchi M: Precise distribution of neuronal nitric oxide synthase mRNA in the rat brain revealed by non-radioisotopic in situ hybridization. Mol Brain Res 53: 1-12, 1998.
17. Garthwaite J: Glutamate, nitric oxide and cell-cell signalling in the nervous system. TiNS 14: 60-67, 1991.
18. McNaught KSP and Brown GC: Nitric oxide causes glutamate release from rat synaptosomes. J Neurochem 70: 1541-1546, 1998.
19. Sequcira SM, Ambrosio AF, Malva JO, Carvalho AP and Carvalho CM: Modulation of glutamate release from rat hippocampal synaptosomes. Nitric Oxide 1: 315-329, 1997.
20. Lei SZ, Pan Z, Aggarwal SK, Chen HV, Hartman J, Sucher NJ and Lipton SA: Effect of nitric oxide production on the redox modulatory site of the NMDA receptor-channel complex. Neuron 8: 1087-1099, 1992.
21. Lipton SA, Choi Y, Pan Z, Lei SZ, Chen HV, Sucher NJ, Loscalzo J, Singel DJ and Stamler JS: A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364: 626-632, 1993.
22. Manzoni O and Bockaert J: Nitric oxide synthase activity endogenously modulates NMDA receptors. J Neurochem 61: 368-370, 1993.
23. Nanri K, Takizawa S, Fujita H, Ogawa S and Shinoara Y: Modulation of extracellular glutamate concentration by nitric oxide synthase inhibitor in rat transient forebrain ischemia. Brain Res 738: 243-248, 1996.
24. Beckman JS: The double-edged role of nitric oxide in brain function and superoxide-mediated injury. J Dev Physiol 15: 53-59, 1991.
25. Zhang F and Iadecola C: Nitroprusside improves blood flow and reduces brain damage after focal ischemia. Neuroreport 4: 559-562, 1993.
26. Zhang F, Benveniste H, Klitzman B and Piantadosi CL: Nitric oxide synthase inhibition and extracellular glutamate concentration after cerebral ischemia/reperfusion. Brain Res 610: 57-61, 1993.
27. Bains JS and Ferguson AV: Nitric oxide regulates NMDA-driven GABAergic inputs to type I neurones of the rat paraventricular nucleus. J Physiol 499: 733-746,1997.
28. 3H]γ-aminobutyric acid in rat hippocampal synaptosomes. Mol Brain Res 55: 337-340, 1998.
29. Tasker JG and Dudek FE: Local inhibitor synaptic inputs to neurones of the paraventricular nucleus in slices of rat hypothalamus. J Physiol 469: 179-192, 1993.
30. Bernardi PS, Valtschanoff JG, Weinberg RJ, Schmidt HH and Rustioni A: Synaptic interactions between primary afferent terminals and GABA and nitric oxide-synthesizing neurones in superficial laminae of the rat spinal cord. J Neurosci 15: 1363-1371, 1995.
31. Gabbott PLA and Bacon SJ: An oriented framework of neuronal processes in the ventral geniculate nucleus of the rat demonstrated by NADPH histochemistry and GABA immunocytochemistry. Neuroscience 60: 417-440, 1994.
32. Lovick TA and Key BJ: Inhibitory effect of nitric oxide on neuronal activity in the periaqueductal grey matter of the rat. Exp Brain Res 108: 382-388, 1996.
33. Valtschanoff JG, Weinberg RJ, Rustioni A and Schmidt HH: Co-localization of neuronal nitric oxide synthase with GABA in rat cuneate nucleus. J Neurocytol 24: 237-245, 1995.
34. Kano T, Shimizu-Sasamata M, Huang PL, Moskowitz MA and Lo EH: Effects of nitric oxide synthase gene knockout on neurotransmitter release in vivo. Neuroscience 86: 695-699, 1998.
35. de Vente J, Markerink-van Ittersum M, Axer H and Steinbusch HW: Nitric oxide-induced cGMP synthesis in cholinergic neurones in the rat brain. Exp Brain Res 136: 480-491, 2001.
36. Lonart G, Wang J and Johnson KM: Nitric oxide induces neurotransmitter release from hippocampal slices. Eur J Pharmacol 220: 271-272, 1992.
37. Suzuki T, Nakajima K, Fujimoto K, Fujii T, Takita M, Kanedo H, Suzuki SS and Akamatsu M: Lasting effect of NO on glutamate release in rat striatum revealed by continuous brain dialysis. NeuroReport 8: 567-570, 1997.
38. Prast H, Tran MH, Fisher H and Philippu A: Nitric oxide-induced release of acetylcholine in the nucleus accumbens: role of cyclic GMP, glutamate and GABA. J Neurochem 71: 266-273, 1998.
39. 3H]dopamine from rat striatum in vitro. J Neurochem 66: 131-137, 1996.
40. Lorrain DS and Hull EM: Nitric oxide increases dopamine and serotonin release in the medial preoptic area. Neuroreport 5: 87-89, 1993.
41. Smith JCE and Whitton PS: The regulation of NMDA-evoked dopamine release by nitric oxide in the frontal cortex and raphe nuclei of freely moving rat. Brain Res 889: 57-62, 2001.
42. Satoh S, Kimura T, Toda M, Miyazaki H, Ono S, Narita H, Murayama T and Nomura Y: NO donors stimulates noradrenaline release from rat hippocampus in a calmodulin-dependent manner in the presence of L-cysteine. J Cell Physiol 169: 87-96, 1996.
43. Lauth D, Hertting G and Jackisch R: 3,4-Diaminopyridine-evoked noradrenaline release in rat hippocampal slices: facilitation by endogenous or exogenous nitric oxide. Brain Res 692: 174-182, 1995.
44. Montague PR, Ganvayco CD, Winn MJ, Marchase RB and Friendlnder MJ: Role of production in NMDA-receptor-mediated neurotransmitter release in cerebral cortex. Science 263: 973-977, 1994.
45. Guevara-Guzman R, Emson PC and Kendrick KM: Modulation of in vivo striatal transmitter release by nitric oxide and cyclic GMP. J Neurochem 62: 807-810, 1994.
46. Kaehler ST, Singewald N, Sinner C and Philippu A: Nitric oxide modulates the release of serotonin in the rat hypothalamus. Brain Res 835: 346-349, 1999.
47. Singewald N and Philippu A: Release of neurotransmitters in the locus coeruleus. Progr Neurobiol 65: 237-267, 1998.
48. Buisson A, Lakhmeche N, Verrecchia C, Plotkine M and Boulu RG: Nitric oxide: and endogenous anticonvulsant substance. Neuroreport 4: 444-446, 1993.
49. Boda B and Szente M: Nitric oxide synthase inhibitor facilitates focal seizures induced by aminopyridine in rat. Neurosci Lett 209: 37-40, 1996.
50. Kabuto H, Yokoi I, Habu H, Willmore LJ, Mori A and Ogawa N: Reduction of nitric oxide synthase activity with development of an epileptogenic focus induced by ferric chloride in the rat brain. Epilepsy Res 25: 65-68, 1996.
51. Przegalinski E, Baran L and Siwanowicz J: The role of nitric oxide in chemically- and electrically-induced seizures in mice. Neurosci Lett 217: 145-148, 1996.
52. Herberg LJ, Grottick A and Rose IC: Nitric oxide synthesis, epileptic seizures and kindling. Psycopharmacol 119: 115-123, 1995.
53. Urbanska EM, Drelewska E, Borowicz KK, Blaszczak P, Kleinrok Z and Czuczwar SJ: NG-nitro-L-arginine, a nitric oxide synthase inhibitor, and seizure susceptibility in four seizure models in mice. J Neural Transm 103: 1145-1152, 1996.
54. Pereira de Vasconcelos A, Gizard F, Marescaux C and Nehlig A: Role of nitric oxide in pentylenetrazol-induced seizures: age-dependent effects in the immature rat. Epilepsia 41: 363-371, 2000.
55. Manzoni O, Prezeau L, Marin P, Deshager S, Bockaert J and Fagni L: Nitric oxide-induced blockade of NMDA receptors. Neuron 8: 653-662, 1992.
56. Boulton CL, Irving AJ, Southam E, Potier B, Garthwaite J and Coillingridge GL: The nitric oxide-cyclic GMP pathway and synaptic depression in rat hippocampal slices. Eur J Neurosci 6: 1528-1535, 1994.
57. Lu W, Chen G and Cheng JS: NMDA antagonist displays anticonvulsant effect via NO synthesis inhibition penicillin-treated rat hippocampal slices. Neuroreport 9: 4045-4049, 1998.
58. Tsuda M, Suzuki T and Misawa M: Aggravation of DMCM-induced seizures by nitric oxide synthase inhibition in mice. Life Sciences 60: 339-343, 1997.
59. Ferraro G, Montalbano ME and La Grutta V: Nitric oxide and glutamate interaction in the control of cortical and hippocampal excitability. Epilepsia 40: 830-836, 1999.
60. Getting SJ, Segieth J, Ahmad S, Biggs CS and Whitton PS: Biphasic modulation of GABA release by nitric oxide in the hippocampus of freely moving rats in vivo. Brain Res 717: 196-199, 1996.
61. Kirkby DR, Carrol DM, Grossman AB and Subramanian S: Factors determining proconvulsant and anticonvulsant effects of inhibitors of nitric oxide synthase in rodents. Epilepsy Res 24: 91-100, 1996.
62. Xiong H, Yamada K, Jourdi H, Kawamura M, Takei N, Han D, Nabeshima T and Nawa H: Regulation of nerve growth factor release by nitric oxide through cyclic GMP pathway in cortical glial cells. Mol Pharmacol 56: 339-347, 1999.
63. Lam HHD, Bhardwaj A, O'Connel MT, Hanley DF, Traystman RJ and Sofroniew MV: Nerve growth factor rapidly suppresses basal, NMDA-evoked, and AMPA-evoked nitric oxide synthase activity in rat hippocampus in vivo. Neurobiology 95: 10926-10931, 1998.
64. Calzà L, Giardino L, Giuliani A, Aloe L and Levi-Montalcini R: Nerve growth factor control of neuronal expression of angiogenetic and vasoactive factors. Proc Natl Acad Sci USA 98: 4160-4165, 2001.
65. Penix LP, Davis W and Subramanian S: Inhibition of NO synthase increases the severity of kainic acid-induced seizures in rodents. Epilepsy Res 18: 177-184, 1994.
66. Rigaud-Monnet AS, Pinard E, Borredon J and Seylaz J: Blockade of nitric oxide synthesis inhibits hippocampal hyperemia in kainic acid-induced seizures. J Cereb Blood Flow 14: 581-590, 1994.
67. Rondouin G, Bockaert J and Lerner-Natoli M: L-Nitroarginine an inhibitor of NO synthase dramatically worsen limbic epilepsy in rats. Neuroreport 4: 1187-1190, 1993.
68. Bitterman N and Bitterman H: L-arginine-NO pathway and CNS oxygen toxicity. J Appl Physiol 84: 1633-1638, 1998.
69. Yasuda H, Fujii M, Fujisawa H, Ito H and Suzuki M: Changes in nitric oxide synthesis and epileptic activity in the contralateral hippocampus of rats following intrahippocampal kainate injection. Epilepsia 42: 13-20, 2001.
70. Lamas S, Pérez-Sala D and Moncada S: Nitric oxide: from discovery to the clinic. TiPS 19: 436-438, 1998.
71. Stringer JL and Erden F: In the hippocampus in vivo, nitric oxide does not appear to function as antiepileptic agent. Exp Brain Res 105: 391-401, 1995.
72. Talavera E, Martinez-Lorenzana G, Corkidi G, Leon-Olea M and Condes-Lara M: NADPH-diaphorase-stained neurons after experimental epilepsy in rats. Nitric Oxide 1: 484-493, 1997.
73. Ferraro G, Sardo P, Di Giovanni G, Di Maio R and La Grutta V: Involvement of nitric oxide in maximal dentate gyrus activation, in the rat. Pflügers Arch - Eur J Physiol, in press, 2004.
74. Quesada O, Hirsch J, Ben-Ari Y and Bernard C: Redox sites of NMDA receptors can modulate epileptiform activity in hippocampal slices from kainic acid-treated rats. Neurosci Lett 121: 171-174, 1996.
75. Huang Z, Huang PL, Ma J, Meng W, Ayata C, Fishman MC and Moskowitz MA: Enlarged infarcts in endothelial nitric oxide synthase knockout mice are attenuated by nitro-L-arginine. J Cereb Blood Flow Metab 16: 981-987, 1996.
76. Iadecola C: Bright and dark sides of nitric oxide in ischemic brain injury. Trends Neurosci 20: 132-139, 1997.
77. Moncada S, Palmer RMJ and Higgs EA: Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol Rev 43: 109-142, 1991.
78. Iadecola C, Zhang F, Casey R, Nagayama M and Ross ME: Delayed reduction of ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene. J Neurosci 17: 9157-9164, 1997.
79. Castillo J, Rama R and Dàvalos A: Nitric oxide-related brain damage in acute ischemic stroke. Stroke 31: 852-860, 2000.
80. Elibol B, Söylemezoglu F, Ünal I, Fujii M, Hirt L, Huang PL, Moskowitz MA and Dalkara T: Nitric oxide is involved in ischemia-induced apoptosis in brain: a study in neuronal nitric oxide synthase null mice. Neuroscience 105: 79-86, 2001.
81. Law A, Gauthier S and Quirion R: Say NO to Alzheimer's disease: the putative links between nitric oxide and dementia of the Alzheimer's type. Brain Res Rev 35: 73-96, 2001.
82. Das I, Khan NS, Puri BK and Hirsch SR: Elevated endogenous nitric oxide synthase inhibitor in schizophrenic plasma may reflect abnormalities in brain nitric oxide production. Neurosci Lett 215: 209-211, 1996.
83. Marras RA, Martins AP, Del Bel EA and Guimaraes FS: L-NOArg, an inhibitor of nitric oxide synthase, induces catalepsy in mice. Neuroreport 7: 158-160, 1995.
84. Wallace MN, Tayebjee MH, Rana FS, Farquhar DA and Nyong'o AO: Pyramidal neurones in pathological human motor cortex express nitric oxide synthase. Neurosci Lett 212: 187-190, 1996.
85. Demas GE, Eliasson MJ, Dawson TM, Dawson VL, Kriegsfeld LJ, Nelson RJ and Snyder SH: Inhibition of neuronal nitric oxide synthase increases aggressive behavior in mice. Mol Medicine 3: 610-616, 1997.
86. La Grutta V and Sabatino M: Focal hippocampal epilepsy: effect of caudate stimulation. Exp Neurol 99: 38-49, 1988.
87. La Grutta V and Sabatino M: Substantia nigra-mediated anticonvulsant action: a possible role of a dopaminergic component. Brain Res 515: 87-93, 1990.
88. Williams JH, Li YG, Nayak A, Errington ML, Murphy KPSJ and Bliss TVP: The suppression of long term potentiation in rat hippocampus by inhibitors of nitric oxide synthase is temperature and age dependent. Neuron 11: 877-884, 1993.
89. Alabadí JA, Thibault JL, Pinard E, Seylaz J and Lasbennes F: 7-Nitroindazole, a selective inhibitor of nNOS, increases hippocampal extracellular glutamate concentration in status epilepticus induced by kainic acid in rats. Brain Res 839: 305-312, 1999.
90. Pereira de Vasconcelos A, Baldwin RA and Wasterlain CG: Nitric oxide mediates the increase in local cerebral blood flow during focal seizures. Proc Natl Acad Sci USA 92: 3175-3179, 1995.
91. Sandirasegarane L, Mikler JR, Tuckek JM and Sulakhe PV: Enhanced forebrain nitric oxide synthase activity in epileptic fowl. Brain Res 735: 311-313, 1996.
92. Proctor MR, Fornai F, Afshar JK and Gale K: The role of nitric oxide in focally-evoked limbic seizures. Neuroscience 76: 1231-1236, 1997.
93. Murashima YL, Yoshii M and Suzuki J: Role of nitric oxide in the epileptogenesis of EL mice. Epilepsia 41: 195-199, 2000.
94. Huh Y, Heo Y, Park C and Ahn H: Transient induction of neuronal nitric oxide synthase in neurons of rat cerebral cortex after status epilepticus. Neurosci Lett 281: 49-52, 2000.
95. Han D, Yamada K, Senzaki K, Xiong H, Nawa H and Nabeshima T: Involvement of nitric oxide in pentylentetrazole-induced kindling in rats. J Neurochem 74: 792-798, 2000.
96. Borowicz KK, Luszczki J, Kleinrok Z and Czuczwar SJ: 7-Nitroindazole, a nitric oxide synthase inhibitor, enhances the anticonvulsive action of ethosuximide and clonazepam against pentylenetrazol-induced convulsions. J Neural Transm 107: 1117-1126, 2000.