The role of nitric oxide in the inhibitory effect of ghrelin against penicillin-induced epileptiform activity in rat

Neuropeptides

Volumn 43, Issue 4, 2009, Pages 295-302

  Aslan, Ali ^a   Yildirim, Mehmet ^a   Ayyildiz, Mustafa ^a   Güven, Ayla ^a   Agar, Erdal ^a  

^a ONDOKUZ MAYIS UNIVERSITY   (Turkey)

Author keywords

7 NI; Epileptiform activity; Ghrelin; l Arginine; l NAME; NOS

Indexed keywords

7 NITROINDAZOLE; ARGININE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GHRELIN; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; PENICILLIN G;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTICONVULSANT ACTIVITY; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; DISEASE MODEL; DRUG DOSE COMPARISON; ENZYME ACTIVATION; EPILEPSY; EPILEPTIC DISCHARGE; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; TREATMENT OUTCOME;

ACTION POTENTIALS; ANIMALS; ANTICONVULSANTS; ELECTROPHYSIOLOGY; EPILEPSY; GHRELIN; INDAZOLES; INJECTIONS, INTRAVENTRICULAR; MALE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PENICILLINS; RATS; RATS, WISTAR;

RATTUS;

EID: 67650957574     PISSN: 01434179     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.npep.2009.05.005     Document Type: Article

References (65)

1. Ayyildiz M., Coskun S., Yildirim M., and Agar E. The effects of ascorbic acid on penicillin-induced epileptiform activity in rats. Epilepsia 48 7 (2007) 1388-1395
2. Bains J.S., and Ferguson A.V. Nitric oxide regulates NMDA-driven GABAergic inputs to type I neurons of rat paraventricular nucleus. J. Physiol. 499 (1997) 733-746
3. Banks W.A., Tschöp M., Robinson S.M., and Heiman M.L. Extent and direction of ghrelin transport across the blood-brain barrier is determined by its unique primary structure. J. Pharmacol. Exp. Ther. 302 2 (2002) 822-827
4. Berilgen M.S., Mungen B., Ustundag B., and Demir C. Serum ghrelin levels are enhanced in patients with epilepsy. Seizure 15 2 (2006) 106-111
5. Bijak M., and Smialowska M. Effects of neuropeptide Y on evoked potentials in the CA1 region and the dentate gyrus of the rat hippocampal slice. Pol. J. Pharmacol. 47 4 (1995) 333-338
6. Bosnak M., Ayyildiz M., Yildirim M., and Agar E. The role of nitric oxide in the anticonvulsant effects of pyridoxine on penicillin-induced epileptiform activity in rats. Epilepsy Res. 76 1 (2007) 49-59
7. Bredt D.S., Glatt C.E., Hwang P.M., Fotuhi M., Dawson T.M., and Snyder S.H. Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron 7 4 (1991) 615-624
8. Buisson A., Lackhmeche N., Verrecia C., Plotkine M., and Bolou R.G. Nitric oxide: an endogenous anticonvulsant substance. Neuroreport 4 (1993) 444-446
9. Camina J.P., Carreira M.C., El Messari S., Llorens-Cortes C., Smith R.G., and Casanueva F.F. Desensitization and endocytosis mechanisms of ghrelin-activated growth hormone secretagogue receptor 1a. Endocrinology 145 2 (2004) 930-940
10. Collins R.C. Kindling of neuroanatomic pathways during recurrent focal penicillin seizures. Brain Res. 150 (1978) 503-517
11. Corda M., Orlandi M., Lecca D., Carboni G., Frau V., and Giorgi O. Pentylenetetrazol-induced kindling in rats: effect of GABA function inhibitors. Pharmacol. Biochem. Behav. 40 (1991) 329-333
12. Cowley M.A., Smith R.G., Diano S., Tschöp M., Pronchuk N., Grove K.L., Strasburger C.J., Bidlingmaier M., Esterman M., Heiman M.L., Garcia-Segura L.M., Nillni E.A., Mendez P., Low M.J., Sotonyi P., Friedman J.M., Liu H., Pinto S., Colmers W.F., Cone R.D., and Horvath T.L. The distribution and mechanism of action of ghrelin in the CNS demonstrates a novel hypothalamic circuit regulating energy homeostasis. Neuron 37 4 (2003) 649-661
13. De Smet B., Depoortere I., Moechars D., Swennen Q., Moreaux B., Cryns K., Tack J., Buyse J., Coulie B., and Peeters T.L. Energy homeostasis and gastric emptying in ghrelin knockout mice. J. Pharmacol. Exp. Ther. 316 1 (2006) 431-439
14. Doyle C., Hölscher C., Rowan M.J., and Anwyl R. The selective neuronal NO synthase inhibitor 7-nitro-indazole blocks both long-term potentiation and depotentiation of field EPSPs in rat hippocampal CA1 in vivo. J. Neurosci. 16 1 (1996) 418-424
15. Fernández-Fernández R., Tena-Sempere M., Roa J., Castellano J.M., Navarro V.M., Aguilar E., and Pinilla L. Direct stimulatory effect of ghrelin on pituitary release of LH through a nitric oxide-dependent mechanism that is modulated by estrogen. Reproduction 133 6 (2007) 1223-1232
16. Fernandez-Guardiola A., Martinez A., and Fernandez-Mas R. Repeated penicilin- induced amygdala epileptic focus in freely moving cats. EEG, polysomnographic (23 h recording), and brain mapping study. Epilepsy Res. 22 (1995) 127-136
17. Ferraro G., and Sardo P. Nitric oxide and brain hyperexcitability. In Vivo 18 (2004) 357-366
18. Ferraro G., Montalbano M.E., and La Grutta V. NO and hippocampal epilepsy: an electrophysiological evidence of a new modulatory system. Epilepsia 38 (1997) 190-191
19. Fisher R.S. Animal models of the epilepsies. Brain Res. 14 (1989) 245-278
20. Gaskin F.S., Farr S.A., Banks W.A., Kumar V.B., and Morley J.E. Ghrelin-induced feeding is dependent on nitric oxide. Peptides 24 6 (2003) 913-918
21. Gonzalez-Trujano M.E., Tapia E., Lopez-Meraz L., Navarrete A., Reyes-Ramirez A., and Martinez A. Anticonvulsant effect of Annona diversifolia Saff. and palmitone on penicillin-induced convulsive activity. A behavioral and EEG study in rats. Epilepsia 47 (2006) 1810-1817
22. Greco R., Latini G., Chiarelli F., Iannetti P., and Verrotti A. Leptin, ghrelin, and adiponectin in epileptic patients treated with valproic acid. Neurology 65 11 (2005) 1808-1809
23. Gungor S., Yücel G., Akinci A., Tabel Y., Ozerol I.H., and Yologlu S. The role of ghrelin in weight gain and growth in epileptic children using valproate. J. Child Neurol. 22 12 (2007) 1384-1388
24. Holmes O., Wallace M.N., and Campbell A.M. Comparison of penicillin epileptogenesis in rat somatosensory and motor cortex. Q. J. Exp. Physiol. 72 4 (1987) 439-452
25. Hou Z., Miao Y., Gao L., Pan H., and Zhu S. Ghrelin-containing neuron in cerebral cortex and hypothalamus linked with the DVC of brainstem in rat. Regul. Peptides 134 (2006) 126-131
26. Kamegai J., Tamura H., Shimizu T., Ishii S., Sugihara H., and Wakabayashi I. Chronic central infusion of ghrelin increases hypothalamic neuropeptide Y and Agouti-related protein mRNA levels and body weight in rats. Diabetes 50 11 (2001) 2438-2443
27. Kitazawa T., De Smet B., Depoortere I., Moreaux B., Verbeke K., Tack J., Coulie B., and Peeters T.L. Gastric motor effects of peptide and non-peptide ghrelin agonists in mice in vivo and in vitro. Gut 54 (2005) 1078-1084
28. Kojima M., and Kangawa K. Ghrelin: structure and function. Physiol. Rev. 85 2 (2005) 495-522
29. Kojima M., Hosoda H., Date Y., Nakazato M., Matsuo H., and Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402 6762 (1999) 656-660
30. Korbonits M., Goldstone A.P., Gueorguiev M., and Grossman A.B. Ghrelin - a hormone with multiple functions. Front Neuroendocrinol. 25 1 (2004) 27-68
31. Lawrence C.B., Snape A.C., Baudoin F.M., and Luckman S.M. Acute central ghrelin and GH secretagogues induce feeding and activate brain appetite centers. Endocrinology 143 1 (2002) 155-162
32. Li Y., Wu X., Zhao Y., Chen S., and Owyang C. Ghrelin acts on the dorsal vagal complex to stimulate pancreatic protein secretion. Am. J. Physiol. Gastrointest. Liver Physiol. 90 (2006) G1350-G1358
33. Lu W., Chen G., and Cheng J.S. NMDA antagonist displays anticonvulsant effect via NO synthesis inhibition penicillin-treated rat hippocampal slices. Neuroreport 9 (1998) 4045-4049
34. Macdonald R.L., and Barker J.L. Pentylenetetrazol and penicillin are selective antagonists of GABA-mediated post-synaptic inhibition in cultured mammalian neurones. Nature 267 (1977) 720-721
35. Masuda Y., Tanaka T., Inomata N., Ohnuma N., Tanaka S., Itoh Z., Hosoda H., Kojima M., and Kangawa K. Ghrelin stimulates gastric acid secretion and motility in rats. Biochem. Biophys. Res. Commun. 276 3 (2000) 905-908
36. Matsumura N., Kikuchi-Utsumi K., and Nakaki T. Activities of 7-nitroindazole and 1-(2-(trifluoromethylphenyl)-imidazole independent of neuronal nitric-oxide synthase inhibition. J. Pharmacol. Exp. Ther. 325 2 (2008) 357-362
37. Meldrum B.S. Neurotransmission in epilepsy. Epilepsia 27 Suppl. 1 (1995) S3-S11
38. Moncada S., Higgs A., and Fruchgott R. XIV international union of pharmacology nomenclature in nitric oxide research. Pharmacol. Rev. 49 (1997) 137-142
39. Mulsch A., Buse R., Mordvintcev P.I., Vanin A.F., Nielsen E.O., Scheel-Kruger J., and Olsen S.P. Nitric oxide promotes seizure activity in kainate-treated rats. Neuroreport 5 (1994) 2325-2328
40. Nagaki S., Fukamauchi F., Sakamoto Y., Higuchi H., Miki N., Miki N., Ono M., Sadamatsu M., Kato N., and Osawa M. Upregulation of brain somatostatin and neuropeptide Y following lidocaine-induced kindling in the rat. Brain Res. 852 2 (2000) 470-474
41. Noè F., Pool A.H., Nissinen J., Gobbi M., Bland R., Rizzi M., Balducci C., Ferraguti F., Sperk G., During M.J., Pitkänen A., and Vezzani A. Neuropeptide Y gene therapy decreases chronic spontaneous seizures in a rat model of temporal lobe epilepsy. Brain 131 (2008) 1506-1515
42. Obay B.D., Tasdemir E., Tümer C., Bilgin H.M., and Sermet A. Antiepileptic effects of ghrelin on pentylenetetrazole-induced seizures in rats. Peptides 28 6 (2007) 1214-1219
43. Obay B.D., Taşdemir E., Tümer C., Bilgin H.M., and Atmaca M. Dose dependent effects of ghrelin on pentylenetetrazole-induced oxidative stress in a rat seizure model. Peptides 29 3 (2008) 448-455
44. Orkin R.D., New D.I., Norman D., Chew S.L., Clark A.J., Grossman A.B., and Korbonits M. Rapid desensitisation of the GH secretagogue (ghrelin) receptor to hexarelin in vitro. J. Endocrinol. Invest. 26 8 (2003) 743-747
45. Paul V., and Ekambaram P. Effect of 7-nitroindazole alone and in combination with phenobarbitone and diazepam on picrotoxin-induced convulsions in rats. Indian J. Physiol. Pharmacol. 47 (2003) 400-406
46. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1986), Academic Press, Sydney
47. Penix L.P., Davis W., and Subramaniam S. Inhibition of NO synthase increases the severity of kainic acid-induced seizures in mice. Epilepsy Res. 18 (1994) 177-184
48. Pinilla L., Barreiro M.L., Tena-Sempere M., and Aguilar E. Role of ghrelin in the control of growth hormone secretion in prepubertal rats: interactions with excitatory amino acids. Neuroendocrinology 77 2 (2003) 83-90
49. Reibel S., Benmaamar R., Lê B.T., Larmet Y., Karla S.P., Marescaux C., and Depaulis A. Neuropeptide Y delays hippocampal kindling in the rat. Hippocampus 13 5 (2003) 557-560
50. Reimer M.K., Pacini G., and Ahren B. Dose-dependent inhibition by ghrelin of insulin secretion in the mouse. Endocrinology 144 3 (2003) 916-921
51. Riediger T., Giannini P., Erguven E., and Lutz T. Nitric oxide directly inhibits ghrelin-activated neurons of the arcuate nucleus. Brain Res. 1125 1 (2006) 37-45
52. Rodríguez-Pacheco F., Luque R.M., García-Navarro S., Gracia-Navarro F., Castaño J.P., and Malagón M.M. Ghrelin induces growth hormone (GH) secretion via nitric oxide (NO)/cGMP signaling. Ann. NY Acad. Sci. 1040 (2005) 452-453
53. Rodríguez-Pacheco F., Luque R.M., Tena-Sempere M., Malagón M.M., and Castaño J.P. Ghrelin induces growth hormone secretion via a nitric oxide/cGMP signalling pathway. J. Neuroendocrinol. 20 3 (2008) 406-412
54. Schwarcz R., and Meldrum B. Excitatory aminoacid antagonists provide a therapeutic approach to neurological disorders. Lancet 2 8447 (1985) 140-143
55. Silva A.P., Xapelli S., Pinheiro P.S., Ferreira R., Lourenço J., Cristóvão A., Grouzmann E., Cavadas C., Oliveira C.R., and Malva J.O. Up-regulation of neuropeptide Y levels and modulation of glutamate release through neuropeptide Y receptors in the hippocampus of kainate-induced epileptic rats. J. Neurochem. 93 1 (2005) 163-170
56. Smith S.E., Man C.M., Yip P.K., Tang E., Chapman A.G., and Meldrum B.S. Anticonvulsant effects of 7-nitroindazole in rodents with reflex epilepsy may result from l-arginine accumulation or a reduction in nitric oxide or l-citrulline formation. Brit. J. Pharmacol. 119 (1996) 165-173
57. Stroud L.M., O'Brien T.J., Jupp B., Wallengren C., and Morris M.J. Neuropeptide Y suppresses absence seizures in a genetic rat model. Brain Res. 1033 2 (2005) 151-156
58. Tsuda M., Suzuki T., and Misawa M. Aggravation of DMCM-induced seizure by nitric oxide synthase inhibitors in mice. Life Sci. 60 (1997) PL339-PL343
59. Vezzani A., Rizzi M., Conti M., and Samanin R. Modulatory role of neuropeptides in seizures induced in rats by stimulation of glutamate receptors. J. Nutr. 130 4S Suppl. (2000) 1046S-1048S
60. Woldbye D.P., and Kokaia M. Neuropeptide Y and seizures: effects of exogenously applied ligands. Neuropeptides 38 4 (2004) 253-260
61. Woldbye D.P., Madsen T.M., Larsen P.J., Mikkelsen J.D., and Bolwig T.G. Neuropeptide Y inhibits hippocampal seizures and wet dog shakes. Brain Res. 737 1-2 (1996) 162-168
62. Woldbye D.P., Larsen P.J., Mikkelsen J.D., Klemp K., Madsen T.M., and Bolwig T.G. Powerful inhibition of kainic acid seizures by neuropeptide Y via Y5-like receptors. Nat Med. 3 7 (1997) 761-764
63. Xapelli S., Agasse F., Ferreira R., Silva A.P., and Malva J.O. Neuropeptide Y as an endogenous antiepileptic, neuroprotective and pro-neurogenic peptide. Recent Pat. CNS Drug Discov. 1 3 (2006) 315-324
64. Xu L., Rensing N., Yang X.F., Zhang H.X., Thio L.L., Rothman S.M., Weisenfeld A.E., Wong M., and Yamada K.A. Leptin inhibits 4-aminopyridine- and pentylenetetrazole-induced seizures and AMPAR-mediated synaptic transmission in rodents. J. Clin. Invest. 118 1 (2008) 272-280
65. Yasuda H., Fuji 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 (2001) 13-20