The opposite effect of convulsant drugs on neuronal and endothelial nitric oxide synthase – A possible explanation for the dual proconvulsive/anticonvulsive action of nitric oxide

1. A. J. Duncan and S. J. Heales, Nitric oxide and neurological disorders, Mol. Aspects Med. 26(1–2) (2005) 67–96; https://doi.org/10.1016/j.mam.2004.09.00415722115 Search in Google Scholar

2. R. Stojanovic, Z. Todorovic, Z. Nesic, S. Vuckovic, N. Cerovac-Cosic and M. Prostran, NG-nitro-larginine methyl ester-induced potentiaton of the effect of aminophylline on rat diaphragm: the role of extracellular calcium, J. Pharmacol. Sci. 96(4) (2004) 493–498; https://doi.org/10.1254/jphs.sce04001x15599090 Search in Google Scholar

3. K. Yamamoto, H. Takei, Y. Koyanagi, N. Koshikawa and M. Kobayashi, Presynaptic cell type-dependent regulation of GABAergic synaptic transmission by nitric oxide in rat insular cortex, Neuroscience 284 (2015) 65–77; https://doi.org/10.1016/j.neuroscience.2014.09.06225286388 Search in Google Scholar

4. L. Yassin, S. Radtke-Schuller, H. Asraf, B. Grothe, M. Hershfinkel, I. D. Forsythe and C. Kopp-Scheinpflug, Nitric oxide signaling modulates synaptic inhibition in the superior paraolivary nucleus (SPN) via cGMP-dependent suppression of KCC2, Front. Neural Circuits 8 (2014) Article ID 65 (12 pages); https://doi.org/10.3389/fncir.2014.00065406073124987336 Search in Google Scholar

5. K. M. Boje, Nitric oxide neurotoxicity in neurodegenerative diseases, Front. Biosci. 9 (2004) 763–776; https://doi.org/10.2741/126814766406 Search in Google Scholar

6. O. Akyol, S. S. Zoroglu, F. Armutcu, S. Sahin and A. Gurel, Nitric oxide as a physiopathological factor in neuropsychiatric disorders, In Vivo 18(3) (2004) 377–390. Search in Google Scholar

7. O. Devinsky, A. Vezzani, T. J. O’Brien, N. Jette, I. E. Scheffer, M. de Curtis and P. Perucca, Epilepsy, Nat. Rev. Dis. Primers 4 (2018) Article ID 18024; https://doi.org/10.1038/nrdp.2018.2429722352 Search in Google Scholar

8. G. Ferraro and P. Sardo, Nitric oxide and brain hyperexcitability, In Vivo 18(3) (2004) 357–366. Search in Google Scholar

9. K. Tieu, H. Ischiropoulos and S. Przedborski, Nitric oxide and reactive oxygen species in Parkinson’s disease, IUBMB Life 55(6) (2003) 329–335; https://doi.org/10.1080/152165403200011432012938735 Search in Google Scholar

10. M. Hsu, B. Srinivas, J. Kumar, R. Subramanian and J. Andersen, Glutathione depletion resulting in selective mitochondrial complex I inhibition in dopaminergic cells is via an NO-mediated pathway not involving peroxynitrite: implications for Parkinson’s disease, J. Neurochem. 92(5) (2005) 1091–1103; https://doi.org/10.1111/j.1471-4159.2004.02929.x15715660 Search in Google Scholar

11. D. Hrncic, A. Rasic-Markovic, D. Krstic, D. Macut, D. Djuric and O. Stanojlovic, The role of nitric oxide in homocysteine thiolactone-induced seizures in adult rats, Cell. Mol. Neurobiol. 30(2) (2010) 219–231; https://doi.org/10.1007/s10571-009-9444-919714460 Search in Google Scholar

12. S. H. Snyder, Janus faces of nitric oxide, Nature 364(6438) (1993) 577; https://doi.org/10.1038/364577a08102475 Search in Google Scholar

13. G. Rondouin, M. Lerner-Natoli, O. Manzoni, M. Lafon-Cazal and J. Bockaert, A nitric oxide (NO) synthase inhibitor accelerates amygdala kindling, Neuroreport 3(9) (1992) 805–808; https://doi.org/10.1097/00001756-199209000-000211384771 Search in Google Scholar

14. A. Becker, G. Grecksch and H. Schroder, N^ω-nitro-l-arginine methyl ester interferes with pentylenetetrazol-induced kindling and has no effect on changes in glutamate binding, Brain Res. 688(1–2) (1995) 230–232; https://doi.org/10.1016/0006-8993(95)00565-88542315 Search in Google Scholar

15. P. Tutka, P. Klonowski, J. Dzieciuch, Z. Kleinrok and S. J. Czuczwar, NG-nitro-l-arginine differentially affects glutamate- or kainate-induced seizures, Neuroreport 7(10) (1996) 1605–1608; https://doi.org/10.1097/00001756-199607080-000158904765 Search in Google Scholar

16. E. Przegalinski, L. Baran and J. Siwanowicz, The role of nitric oxide in chemically- and electrically-induced seizures in mice, Neurosci. Lett. 217(2–3) (1996) 145–148.10.1016/0304-3940(96)13085-8 Search in Google Scholar

17. M. S. Starr and B. S. Starr, Do NMDA receptor-mediated changes in motor behaviour involve nitric oxide? Eur. J. Pharmacol. 272(2–3) (1995) 211–217; https://doi.org/10.1016/0014-2999(94)00644-m7713165 Search in Google Scholar

18. E. M. Urbanska, E. Drelewska, K. K. Borowicz, P. Blaszczak, Z. Kleinrok and S. J. Czuczwar NG-nitro-l-arginine, a nitric oxide synthase inhibitor, and seizure susceptibility in four seizure models in mice, J. Neural Transm. (Vienna) 103(10) (1996) 1145–1152; https://doi.org/10.1007/BF012711999013401 Search in Google Scholar

19. L. A. Vega, G. Ceballos and F. Vega-Diaz, Role of nitric oxide synthase on brain GABA transaminase activity and GABA levels, Acta Pharm. 68(3) (2018) 349–359; https://doi.org/10.2478/acph-2018-002231259693 Search in Google Scholar

20. O. Devinsky, A. Vezzani, S. Najjar, N. C. De Lanerolle and M. A. Rogawski, Glia and epilepsy: excitability and inflammation, Trends Neurosci. 36(3) (2013) 174–184; https://doi.org/10.1016/j.tins.2012.11.00823298414 Search in Google Scholar

21. Y. Chen, C. Qin, J. Huang, X. Tang, C. Liu, K. Huang, J. Xu, G. Guo, A. Tong and L. Zhou, The role of astrocytes in oxidative stress of central nervous system: A mixed blessing, Cell. Prolif. 53(3) (2020) e12781; https://doi.org/10.1111/cpr.12781710695132035016 Search in Google Scholar

22. A. Falkowska, I. Gutowska, M. Goschorska, P. Nowacki, D. Chlubek and I. Baranowska-Bosiacka, Energy metabolism of the brain, including the cooperation between astrocytes and neurons, especially in the context of glycogen metabolism, Int. J. Mol. Sci. 16(11) (2015) 25959–25981; https://doi.org/10.3390/ijms161125939466179826528968 Search in Google Scholar

23. D. Boison and C. Steinhauser, Epilepsy and astrocyte energy metabolism, Glia 66(6) (2018) 1235–1243; https://doi.org/10.1002/glia.23247590395629044647 Search in Google Scholar

24. M. De Pitta, N. Brunel and A. Volterra, Astrocytes: Orchestrating synaptic plasticity?, Neuroscience 323 (2016) 43–61; https://doi.org/10.1016/j.neuroscience.2015.04.00125862587 Search in Google Scholar

25. S. M. Q. Hussaini and M. H. Jang, New roles for old glue: astrocyte function in synaptic plasticity and neurological disorders, Int. Neurourol. J. 22(Suppl. 3) (2018) S106–S114; https://doi.org/10.5213/inj.1836214.107623472830396259 Search in Google Scholar

26. A. Volterra and J. Meldolesi, Astrocytes, from brain glue to communication elements: the revolution continues, Nat. Rev. Neurosci. 6(8) (2005) 626–640; https://doi.org/10.1038/nrn172216025096 Search in Google Scholar

27. L. K. Bak, A. Schousboe and H. S. Waagepetersen, The glutamate/GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer, J. Neurochem. 98(3) (2006) 641–653; https://doi.org/10.1111/j.1471-4159.2006.03913.x16787421 Search in Google Scholar

28. N. N. Haj-Yasein, V. Jensen, I. Ostby, S. W. Omholt, J. Voipio, K. Kaila, O. P. Ottersen, O. Hvalby and E. A. Nagelhus, Aquaporin-4 regulates extracellular space volume dynamics during high-frequency synaptic stimulation: a gene deletion study in mouse hippocampus, Glia 60(6) (2012) 867–874; https://doi.org/10.1002/glia.2231922419561 Search in Google Scholar

29. F. Vasile, E. Dossi and N. Rouach, Human astrocytes: structure and functions in the healthy brain, Brain Struct. Funct. 222(5) (2017) 2017–2029; https://doi.org/10.1007/s00429-017-1383-5550425828280934 Search in Google Scholar

30. N. J. Abbott, L. Ronnback and E. Hansson, Astrocyte-endothelial interactions at the blood-brain barrier, Nat. Rev. Neurosci. 7(1) (2006) 41–53; https://doi.org/10.1038/nrn182416371949 Search in Google Scholar

31. Y. Serlin, I. Shelef, B. Knyazer and A. Friedman, Anatomy and physiology of the blood-brain barrier, Semin. Cell Dev. Biol. 38 (2015) 2–6; https://doi.org/10.1016/j.semcdb.2015.01.002439716625681530 Search in Google Scholar

32. G. R. Gordon, S. J. Mulligan and B. A. MacVicar, Astrocyte control of the cerebrovasculature, Glia 55(12) (2007) 1214–1221; https://doi.org/10.1002/glia.2054317659528 Search in Google Scholar

33. C. Iadecola and M. Nedergaard, Glial regulation of the cerebral microvasculature, Nat. Neurosci. 10(11) (2007) 1369–1376; https://doi.org/10.1038/nn200317965657 Search in Google Scholar

34. S. Robel and H. Sontheimer, Glia as drivers of abnormal neuronal activity, Nat. Neurosci. 19(1) (2016) 28–33; https://doi.org/10.1038/nn.4184496616026713746 Search in Google Scholar

35. A. Tabernero, J. P. Bolanos and J. M. Medina, Lipogenesis from lactate in rat neurons and astrocytes in primary culture, Biochem. J. 294(3) (1993) 635–638; https://doi.org/10.1042/bj294063511345088379917 Search in Google Scholar

36. R. F. Squires, E. Saederup, J. N. Crawley, P. Skolnick and S. M. Paul, Convulsant potencies of tetrazoles are highly correlated with actions on GABA/benzodiazepine/picrotoxin receptor complexes in brain, Life Sci. 35(14) (1984) 1439–1444; https://doi.org/10.1016/0024-3205(84)90159-06090836 Search in Google Scholar

37. A. Tourov, R. Ferri, S. Del Gracco, M. Elia, S. A. Musumeci and M. C. Stefanini, Spike morphology in PTZ-induced generalized and cobalt-induced partial experimental epilepsy, Funct. Neurol. 11(5) (1996) 237–245. Search in Google Scholar

38. N. Y. Lukomskaya, N. I. Rukoyatkina, L. V. Gorbunova, V. E. Gmiro and L. G. Magazanik, Studies of the roles of NMDA and AMPA glutamate receptors in the mechanism of corasole convulsions in mice, Neurosci. Behav. Physiol. 34(8) (2004) 783–789; https://doi.org/10.1023/b:neab.0000038128.02725.7e15587806 Search in Google Scholar

39. X. Zhu, J. Dong, B. Han, R. Huang, A. Zhang, Z. Xia, H. Chang, J. Chao and H. Yao, Neuronal nitric oxide synthase contributes to PTZ kindling epilepsy-induced hippocampal endoplasmic reticulum stress and oxidative damage, Front. Cell. Neurosci. 11 (2017) Article ID 377 (16 pages); https://doi.org/10.3389/fncel.2017.00377571233729234274 Search in Google Scholar

40. A. Morales-Villagran and R. Tapia, Preferential stimulation of glutamate release by 4-aminopyri-dine in rat striatum in vivo, Neurochem. Int. 28(1) (1996) 35–40; https://doi.org/10.1016/0197-0186(95)00064-f8746762 Search in Google Scholar

41. L. Medina-Ceja, A. Morales-Villagran and R. Tapia, Action of 4-aminopyridine on extracellular amino acids in hippocampus and entorhinal cortex: a dual microdialysis and electroencehalo-graphic study in awake rats, Brain Res. Bull. 53(3) (2000) 255–262; https://doi.org/10.1016/s0361-9230(00)00336-111113578 Search in Google Scholar

42. F. Pena and R. Tapia, Relationships among seizures, extracellular amino acid changes, and neuro-degeneration induced by 4-aminopyridine in rat hippocampus: a microdialysis and electroencephalographic study, J. Neurochem. 72(5) (1999) 2006–2014; https://doi.org/10.1046/j.1471-4159.1999.0722006.x10217278 Search in Google Scholar

43. F. Pena and R. Tapia, Seizures and neurodegeneration induced by 4-aminopyridine in rat hippo-campus in vivo: role of glutamate- and GABA-mediated neurotransmission and of ion channels, Neuroscience 101(3) (2000) 547–561; https://doi.org/10.1016/s0306-4522(00)00400-011113304 Search in Google Scholar

44. D. R. Curtis, A. W. Duggan, D. Felix and G. A. Johnston, GABA, bicuculline and central inhibition, Nature 226(5252) (1970) 1222–1224; https://doi.org/10.1038/2261222a04393081 Search in Google Scholar

45. V. Seutin and S. W. Johnson, Recent advances in the pharmacology of quaternary salts of bicucul-line, Trends Pharmacol. Sci. 20(7) (1999) 268–270; https://doi.org/10.1016/s0165-6147(99)01334-610390643 Search in Google Scholar

46. W. P. Arnold, C. K. Mittal, S. Katsuki and F. Murad, Nitric oxide activates guanylate cyclase and increases guanosine 3’:5’-cyclic monophosphate levels in various tissue preparations, Proc. Natl. Acad. Sci. USA 74(8) (1977) 3203–3207; https://doi.org/10.1073/pnas.74.8.320343149820623 Search in Google Scholar

47. J. Garthwaite, Glutamate, nitric oxide and cell-cell signalling in the nervous system, Trends Neurosci. 14(2) (1991) 60–67; https://doi.org/10.1016/0166-2236(91)90022-m1708538 Search in Google Scholar

48. J. Garthwaite, Nitric oxide signalling in the nervous system, Semin. Neurosci. 5 (1993) 171–180.10.1016/S1044-5765(05)80050-8 Search in Google Scholar

49. J. Garthwaite, S. L. Charles and R. Chess-Williams, Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain, Nature 336(6197) (1988) 385–388; https://doi.org/10.1038/336385a02904125 Search in Google Scholar

50. A. Klaassen, J. Glykys, J. Maguire, C. Labarca, I. Mody and J. Boulter, Seizures and enhanced cortical GABAergic inhibition in two mouse models of human autosomal dominant nocturnal frontal lobe epilepsy, Proc. Natl. Acad. Sci. USA 103(50) (2006) 19152–19157; https://doi.org/10.1073/pnas.0608215103168135117146052 Search in Google Scholar

51. I. Cohen, V. Navarro, S. Clemenceau, M. Baulac and R. Miles, On the origin of interictal activity in human temporal lobe epilepsy in vitro, Science 298(5597) (2002) 1418–1421; https://doi.org/10.1126/science.107651012434059 Search in Google Scholar

52. F. Jensen, Developmental factors regulating susceptibility to perinatal brain injury and seizures, Curr. Opin. Pediatr. 18(6) (2006) 628–633; https://doi.org/10.1097/MOP.Ob013e328010c536 Search in Google Scholar

53. Y. Ben-Ari, C. Rovira, J.L. Gaiarsa, R. Corradetti, O. Robain and E. Cherubini, GABAergic mechanisms in the CA3 hippocampal region during early postnatal life, Prog. Brain Res. 83 (1990) 313–321; https://doi.org/10.1016/s0079-6123(08)61259-52168059 Search in Google Scholar

54. S. Zanelli, M. Naylor and J. Kapur, Nitric oxide alters GABAergic synaptic transmission in cultured hippocampal neurons, Brain Res. 1297 (2009) 23–31; https://doi.org/10.1016/j.brainres.2009.08.044279299019699726 Search in Google Scholar

55. Z. Huang, P. L. Huang, J. Ma, W. Meng, C. Ayata, M. C. Fishman, and M. A. Moskowitz, Enlarged infarcts in endothelial nitric oxide synthase knockout mice are attenuated by nitro-l-arginine, J. Cereb. Blood Flow Metab. 16(5) (1996) 981–987; https://doi.org/10.1097/00004647-199609000-000238784243 Search in Google Scholar

56. E. Morikawa, M. A. Moskowitz, Z. Huang, T. Yoshida, K. Irikura and T. Dalkara, l-arginine infusion promotes nitric oxide-dependent vasodilation, increases regional cerebral blood flow, and reduces infarction volume in the rat, Stroke 25(2) (1994) 429–435; https://doi.org/10.1161/01.str.25.2.4297508154 Search in Google Scholar

57. M. Endres, U. Laufs, Z. Huang, T. Nakamura, P. Huang, M. A. Moskowitz and J. K. Liao, Stroke protection by 3-hydroxy-3-methylglutaryl (HMG)-CoA reducta se inhibitors mediated by endothelial nitric oxide synthase, Proc. Natl. Acad. Sci. USA 95(15) (1998) 8880–8885; https://doi.org/10.1073/pnas.95.15.8880211719671773 Search in Google Scholar

58. K. Iwase, K. Miyanaka, A. Shimizu, A. Nagasaki, T. Gotoh, M. Mori and M. Takiguchi, Induction of endothelial nitric-oxide synthase in rat brain astrocytes by systemic lipopolysaccharide treatment, J. Biol. Chem. 275(16) (2000) 11929–11933; https://doi.org/10.1074/jbc.275.16.1192910766821 Search in Google Scholar

59. J. L. Dinerman, T. M. Dawson, M. J. Schell, A. Snowman and S. H. Snyder, Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: implications for synaptic plasticity, Proc. Natl. Acad. Sci. USA 91(10) (1994) 4214–4218; https://doi.org/10.1073/pnas.91.10.4214437557514300 Search in Google Scholar

60. A. Caviedes, M. Varas-Godoy, C. Lafourcade, S. Sandoval, J. Bravo-Alegria, T. Kaehne, A. Mass-mann, J. P. Figueroa, F. Nualart and U. Wyneken, Endothelial nitric oxide synthase is present in dendritic spines of neurons in primary cultures, Front. Cell. Neurosci. 11 (2017) Article ID 180; https://doi.org/10.3389/fncel.2017.00180549583128725180 Search in Google Scholar