Involvement of the nitrergic system in the proconvulsant effect of social isolation stress in male mice

Epilepsy and Behavior

Volumn 41, Issue , 2014, Pages 158-163

  Amiri, Shayan ^a,b   Shirzadian, Armin ^a,b   Haj Mirzaian, Arya ^a,b   Imran Khan, Muhammad ^c   Balaei, Maryam Rahimi ^d   Kordjazy, Nastaran ^a,b   Dehpour, Ahmad Reza ^a,b   Mehr, Shahram Ejtemaei ^a,b  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Mice; Nitric oxide; PTZ clonic seizure model; Social isolation; Stress

Indexed keywords

AMINOGUANIDINE; ARGININE; CORTICOSTERONE; INDUCIBLE NITRIC OXIDE SYNTHASE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRITE; PENTETRAZOLE; CONVULSANT AGENT; ENZYME INHIBITOR; NITRIC OXIDE SYNTHASE;

AFFECT; ANIMAL EXPERIMENT; ARTICLE; CHRONIC STRESS; CLONIC SEIZURE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; FORCED SWIM TEST; HIPPOCAMPUS; HOLE BOARD TEST; MALE; MODULATION; MOUSE; NEUROENDOCRINE SYSTEM; NITRERGIC NERVE; NONHUMAN; OPEN FIELD TEST; PERINATAL PERIOD; SEIZURE SUSCEPTIBILITY; SEIZURE THRESHOLD; SOCIAL ISOLATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICALLY INDUCED; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; MENTAL STRESS; METABOLISM; SEIZURES;

ANIMALS; ARGININE; CONVULSANTS; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; HIPPOCAMPUS; MALE; MICE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PENTYLENETETRAZOLE; SEIZURES; SOCIAL ISOLATION; STRESS, PSYCHOLOGICAL;

EID: 84908446954     PISSN: 15255050     EISSN: 15255069     Source Type: Journal    
DOI: 10.1016/j.yebeh.2014.09.080     Document Type: Article

References (50)

1. McCagh J., Fisk J.E., Baker G.A. Epilepsy, psychosocial and cognitive functioning. Epilepsy Res 2009, 86:1-14.
2. Maguire J., Salpekar J.A. Stress, seizures, and hypothalamic-pituitary-adrenal axis targets for the treatment of epilepsy. Epilepsy Behav 2013, 26:352-362.
3. Charyton C., Elliott J.O., Lu B., Moore J.L. The impact of social support on health related quality of life in persons with epilepsy. Epilepsy Behav 2009, 16:640-645.
4. Fone K.C., Porkess M.V. Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders. Neurosci Biobehav Rev 2008, 32:1087-1102.
5. Marsden C.A., King M.V., Fone K.C. Influence of social isolation in the rat on serotonergic function and memory-relevance to models of schizophrenia and the role of 5-HT6 receptors. Neuropharmacology 2011, 61:400-407.
6. Koob G.F., Ehlers C.L., Kupfer D.J. Animal models of depression 1989, Birkhauser, Boston.
7. Pacher P., Beckman J.S., Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 2007, 87:315-424.
8. Olivenza R., Moro M.A., Lizasoain I., Lorenzo P., Fernández A.P., Rodrigo J., et al. Chronic stress induces the expression of inducible nitric oxide synthase in rat brain cortex. J Neurochem 2000, 74:785-791.
9. Hölscher C. Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity. Trends Neurosci 1997, 20:298-303.
10. Zhou Q.-G., Zhu L.-J., Chen C., Wu H.-Y., Luo C.-X., Chang L., et al. Hippocampal neuronal nitric oxide synthase mediates the stress-related depressive behaviors of glucocorticoids by downregulating glucocorticoid receptor. J Neurosci 2011, 31:7579-7590.
11. Hu Y., Wu D.-L., Luo C.-X., Zhu L.-J., Zhang J., Wu H.-Y., et al. Hippocampal nitric oxide contributes to sex difference in affective behaviors. Proc Natl Acad Sci 2012, 109:14224-14229.
12. Banach M., Piskorska B., Czuczwar S. Nitric oxide, epileptic seizures, and action of antiepileptic drugs. CNS Neurol Disord Drug Targets 2011, 10:808-819.
13. Watanabe M., Miyai A., Danjo S., Nakamura Y., Itoh K. The threshold of pentylenetetrazole-induced convulsive seizures, but not that of nonconvulsive seizures, is controlled by the nitric oxide levels in murine brains. Exp Neurol 2013, 247:645-652.
14. Zhou Q.G., Hu Y., Hua Y., Hu M., Luo C.X., Han X., et al. Neuronal nitric oxide synthase contributes to chronic stress-induced depression by suppressing hippocampal neurogenesis. J Neurochem 2007, 103:1843-1854.
15. Harvey B.H., Oosthuizen F., Brand L., Wegener G., Stein D.J. Stress-restress evokes sustained iNOS activity and altered GABA levels and NMDA receptors in rat hippocampus. Psychopharmacology (Berl) 2004, 175:494-502.
16. Salzberg M., Kumar G., Supit L., Jones N.C., Morris M.J., Rees S., et al. Early postnatal stress confers enduring vulnerability to limbic epileptogenesis. Epilepsia 2007, 48:2079-2085.
17. Kovács R., Rabanus A., Otáhal J., Patzak A., Kardos J., Albus K., et al. Endogenous nitric oxide is a key promoting factor for initiation of seizure-like events in hippocampal and entorhinal cortex slices. J Neurosci 2009, 29:8565-8577.
18. Löscher W., Hönack D., Fassbender C.P., Nolting B. The role of technical, biological and pharmacological factors in the laboratory evaluation of anticonvulsant drugs. III. Pentylenetetrazole seizure models. Epilepsy Res 1991, 8:171-189.
19. Chadda R., Devaud L.L. Sex differences in effects of mild chronic stress on seizure risk and GABA A receptors in rats. Pharmacol Biochem Behav 2004, 78:495-504.
20. Matsumoto K., Nomura H., Murakami Y., Taki K., Takahata H., Watanabe H. Long-term social isolation enhances picrotoxin seizure susceptibility in mice: up-regulatory role of endogenous brain allopregnanolone in GABAergic systems. Pharmacol Biochem Behav 2003, 75:831-835.
21. Joëls M. Stress, the hippocampus, and epilepsy. Epilepsia 2009, 50:586-597.
22. Bahremand A., Nasrabady S.E., Shafaroodi H., Ghasemi M., Dehpour A.R. Involvement of nitrergic system in the anticonvulsant effect of the cannabinoid CB1 agonist ACEA in the pentylenetetrazole-induced seizure in mice. Epilepsy Res 2009, 84:110-119.
23. Homayoun H., Khavandgar S., Namiranian K., Gaskari S.A., Dehpour A.R. The role of nitric oxide in anticonvulsant and proconvulsant effects of morphine in mice. Epilepsy Res 2002, 48:33-41.
24. Takeda H., Tsuji M., Matsumiya T. Changes in head-dipping behavior in the hole-board test reflect the anxiogenic and/or anxiolytic state in mice. Eur J Pharmacol 1998, 350:21-29.
25. Porsolt R., Bertin A., Jalfre M. Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 1977, 229:327-336.
26. Haj-Mirzaian A., Hamzeh N., Javadi-Paydar M., Abdollahzadeh Estakhri M.R., Dehpour A.R. Resistance to depression through interference of opioid and nitrergic systems in bile-duct ligated mice. Eur J Pharmacol 2013, 708:38-43.
27. Bahremand A., Nasrabady S.E., Ziai P., Rahimian R., Hedayat T., Payandemehr B., et al. Involvement of nitric oxide-cGMP pathway in the anticonvulsant effects of lithium chloride on PTZ-induced seizure in mice. Epilepsy Res 2010, 89:295-302.
28. Ding J., Li Q.Y., Wang X., Sun C.H., Lu C.Z., Xiao B.G. Fasudil protects hippocampal neurons against hypoxia-reoxygenation injury by suppressing microglial inflammatory responses in mice. J Neurochem 2010, 114:1619-1629.
29. Veenema A.H., Meijer O.C., de Kloet E.R., Koolhaas J.M., Bohus B.G. Differences in basal and stress-induced HPA regulation of wild house mice selected for high and low aggression. Horm Behav 2003, 43:197-204.
30. Droste S.K., de Groote L., Atkinson H.C., Lightman S.L., Reul J.M., Linthorst A.C. Corticosterone levels in the brain show a distinct ultradian rhythm but a delayed response to forced swim stress. Endocrinology 2008, 149:3244-3253.
31. Mechiel Korte S., De Boer S.F. A robust animal model of state anxiety: fear-potentiated behaviour in the elevated plus-maze. Eur J Pharmacol 2003, 463:163-175.
32. Brenes J.C., Padilla M., Fornaguera J. A detailed analysis of open-field habituation and behavioral and neurochemical antidepressant-like effects in postweaning enriched rats. Behav Brain Res 2009, 197:125-137.
33. Wei X.Y., Yang J.Y., Dong Y.X., Wu C.F. Anxiolytic-like effects of oleamide in group-housed and socially isolated mice. Prog Neuropsychopharmacol Biol Psychiatry 2007, 31:1189-1195.
34. Crawley J.N. Exploratory behavior models of anxiety in mice. Neurosci Biobehav Rev 1985, 9:37-44.
35. Gould T.D., Gould T. Mood and anxiety related phenotypes in mice: characterizing using behavioral tests 2009, Humana Press, New York, NY.
36. Evans J., Sun Y., McGregor A., Connor B. Allopregnanolone regulates neurogenesis and depressive/anxiety-like behaviour in a social isolation rodent model of chronic stress. Neuropharmacology 2012, 63:1315-1326.
37. Kokare D.M., Dandekar M.P., Singru P.S., Gupta G.L., Subhedar N.K. Involvement of α-MSH in the social isolation induced anxiety- and depression-like behaviors in rat. Neuropharmacology 2010, 58:1009-1018.
38. Hawkley L.C., Cole S.W., Capitanio J.P., Norman G.J., Cacioppo J.T. Effects of social isolation on glucocorticoid regulation in social mammals. Horm Behav 2012, 62:314-323.
39. Lukkes J.L., Mokin M.V., Scholl J.L., Forster G.L. Adult rats exposed to early-life social isolation exhibit increased anxiety and conditioned fear behavior, and altered hormonal stress responses. Horm Behav 2009, 55:248-256.
40. Mutlu O., Ulak G., Laugeray A., Belzung C. Effects of neuronal and inducible NOS inhibitor 1-[2-(trifluoromethyl) phenyl] imidazole (TRIM) in unpredictable chronic mild stress procedure in mice. Pharmacol Biochem Behav 2009, 92:82-87.
41. Zlatković J., Bernardi R.E., Filipović D. Protective effect of Hsp70i against chronic social isolation stress in the rat hippocampus. J Neural Transm 2014, 121:3-14.
42. Itoh K., Watanabe M., Yoshikawa K., Kanaho Y., Berliner L., Fujii H. Magnetic resonance and biochemical studies during pentylenetetrazole-kindling development: the relationship between nitric oxide, neuronal nitric oxide synthase and seizures. Neuroscience 2004, 129:757-766.
43. Rundfeldt C., Koch R., Richter A., Mevissen M., Gerecke U., Löscher W. Dose-dependent anticonvulsant and proconvulsant effects of nitric oxide synthase inhibitors on seizure threshold in a cortical stimulation model in rats. Eur J Pharmacol 1995, 274:73-81.
44. Russo E., Chimirri S., Aiello R., De Fazio S., Leo A., Rispoli V., et al. Lamotrigine positively affects the development of psychiatric comorbidity in epileptic animals, while psychiatric comorbidity aggravates seizures. Epilepsy Behav 2013, 28:232-240.
45. Herberg L., Grottick A., Rose I. Nitric oxide synthesis, epileptic seizures and kindling. Psychopharmacology (Berl) 1995, 119:115-123.
46. -/-) before and after pentylenetetrazole kindling. Pharmacol Biochem Behav 2006, 85:804-812.
47. Nelson R.J., Chiavegatto S. Molecular basis of aggression. Trends Neurosci 2001, 24:713-719.
48. Matsumoto K., Puia G., Dong E., Pinna G. GABAA receptor neurotransmission dysfunction in a mouse model of social isolation-induced stress: possible insights into a non-serotonergic mechanism of action of SSRIs in mood and anxiety disorders. Stress 2007, 10:3-12.
49. Miczek K.A., Fish E.W., Joseph F., De Almeida R.M. Social and neural determinants of aggressive behavior: pharmacotherapeutic targets at serotonin, dopamine and γ-aminobutyric acid systems. Psychopharmacology (Berl) 2002, 163:434-458.
50. Cacioppo J.T., Hawkley L.C. Perceived social isolation and cognition. Trends Cogn Sci 2009, 13:447-454.