Apigenin reverses behavioural impairments and cognitive decline in kindled mice via CREB-BDNF upregulation in the hippocampus

References

• Manford M. Recent advances in epilepsy. J Neurol 2017;264:1811–24. doi: 10.1007/s00415-017-8394-2
   PubMed Web of Science ®Google Scholar
• Jacobs MP, Leblanc GG, Brooks-Kayal A, Jensen FE, Lowenstein DH, Noebels JL, et al. Curing epilepsy: progress and future directions. Epilepsy Behav 2009;14:438–45. doi: 10.1016/j.yebeh.2009.02.036
   PubMed Web of Science ®Google Scholar
• Reddy DS, Kuruba R. Experimental models of status epilepticus and neuronal injury for evaluation of therapeutic interventions. Int J Mol Sci 2013;14:18284–318. doi: 10.3390/ijms140918284
   PubMed Web of Science ®Google Scholar
• Ramalingam R, Nath AR, Madhavi BB, Nagulu M, Balasubramaniam A. Free radical scavenging and antiepileptic activity of Leucas lanata. J Pharm Res 2013;6:368–72.
   Google Scholar
• Eddy CM, Rickards HE, Cavanna AE. The cognitive impact of antiepileptic drugs. Ther Adv Neurol Disord 2011;4(6):385–407. doi: 10.1177/1756285611417920
   PubMedGoogle Scholar
• Scott AJ, Sharpe L, Hunt C, Gandy M. Anxiety and depressive disorders in people with epilepsy: a meta analysis. Epilepsia 2017;58(6):973–82. doi: 10.1111/epi.13769
   PubMed Web of Science ®Google Scholar
• Ribot R, Ouyang B, Kanner AM. The impact of antidepressants on seizure frequency and depressive and anxiety disorders of patients with epilepsy: is it worth investigating? Epilepsy Behav 2017;70:5–9. doi: 10.1016/j.yebeh.2017.02.032
   PubMed Web of Science ®Google Scholar
• Mazumder AG, Sharma P, Patial V, Singh D. Crocin attenuates kindling development and associated cognitive impairments in mice via inhibiting reactive oxygen species-mediated NF-kB activation. Basic Clin Pharmacol Toxicol 2017;120:426–33. doi: 10.1111/bcpt.12694
   PubMed Web of Science ®Google Scholar
• Youdim KA, Shukitt-Hale B, Joseph JA. Flavonoids and the brain: interactions at the blood–brain barrier and their physiological effects on the central nervous system. Free Radic Biol Med 2004;37:1683–93. doi: 10.1016/j.freeradbiomed.2004.08.002
   PubMed Web of Science ®Google Scholar
• Ramassamy C. Emerging role of polyphenolic compounds in the treatment of neurodegenerative diseases: a review of their intracellular targets. Eur J Pharmacol 2006;545:51–64. doi: 10.1016/j.ejphar.2006.06.025
   PubMed Web of Science ®Google Scholar
• Hamilton ML, Van Remmen H, Drake JA, Yang H, Guo ZM, Kewitt K, et al. Does oxidative damage to DNA increase with age? Proc Natl Acad Sci 2001;98:10469–74. doi: 10.1073/pnas.171202698
   PubMed Web of Science ®Google Scholar
• Han JY, Ahn SY, Kim CS, Yoo SK, Kim SK, Kim HC, et al. Protection of apigenin against kainate-induced excitotoxicity by anti-oxidative effects. Biol Pharm Bull 2012;35:1440–6. doi: 10.1248/bpb.b110686
   PubMed Web of Science ®Google Scholar
• Avallone R, Zanoli P, Puia G, Kleinschnitz M, Schreier P, Baraldi M. Pharmacological profile of apigenin, a flavonoid isolated from Matricaria chamomilla. Biochem Pharmacol 2000;59:1387–94. doi: 10.1016/S0006-2952(00)00264-1
   PubMed Web of Science ®Google Scholar
• Viola H, Wasowski C, Levi de Stein M, Wolfman C, Silveira R, Dajas F, et al. Apigenin, a component of Matricaria recutita flowers, is a central benzodiazepine receptors-ligand with anxiolytic effects. Planta Med 1995;61:213–6. doi: 10.1055/s-2006-958058
   PubMed Web of Science ®Google Scholar
• Huang RQ, Bell-Horner CL, Dibas MI. Pentylenetetrazole induced inhibition of recombinant gamma-aminobutyric acid type A (GABA(A)) receptors: mechanism and site of action. J Pharmacol Exp Ther 2001;298:986–95.
   PubMed Web of Science ®Google Scholar
• Mortazavi F, Ericson M, Story D, Hulce VD, Dunbar GL. Spatial learning deficits and emotional impairments in pentylenetetrazole-kindled rats. Epilepsy Behav 2005;7:629–38. doi: 10.1016/j.yebeh.2005.08.019
   PubMed Web of Science ®Google Scholar
• Löscher W. Critical review of current animal models of seizures and epilepsy used in the discovery and development of new antiepileptic drugs. Seizure 2011;20:359–68. doi: 10.1016/j.seizure.2011.01.003
   PubMed Web of Science ®Google Scholar
• Dhir A. Pentylenetetrazol (PTZ) kindling model of epilepsy. Curr Protoc Neurosci 2012. Chapter 9: Unit 9.37. doi:10.1002/0471142301.ns0937s58.
   PubMedGoogle Scholar
• Singh D, Mishra A, Goel RK. Effect of saponin fraction from Ficus religiosa on memory deficit, and behavioral and biochemical impairments in pentylenetetrazol kindled mice. Epilepsy Behav 2013;27:206–11. doi: 10.1016/j.yebeh.2012.11.004
   PubMed Web of Science ®Google Scholar
• Singh T, Goel RK. Evidence in support of using a neurochemistry approach to identify therapy for both epilepsy and associated depression. Epilepsy Behav 2016;61:248–57. doi: 10.1016/j.yebeh.2016.05.005
   PubMed Web of Science ®Google Scholar
• Jäger AK, Krydsfeldt K, Rasmussen HB. Bioassay-guided isolation of apigenin with GABA-benzodiazepine activity from Tanacetum parthenium. Phytother Res 2009;23:1642–4. doi: 10.1002/ptr.2816
   PubMed Web of Science ®Google Scholar
• Thilakarathna SH, Rupasinghe HPV. Flavonoid bioavailability and attempts for bioavailability enhancement. Nutrients 2013;5:3367–87. doi: 10.3390/nu5093367
   PubMed Web of Science ®Google Scholar
• Venigalla M, Gyengesi E, Müunch G. Curcumin and apigenin-novel and promising therapeutics against chronic neuroinflammation in Alzheimer’s disease. Neural Regen Res 2015;10:1181–5. doi: 10.4103/1673-5374.162686
   PubMed Web of Science ®Google Scholar
• Singh P, Singh D, Goel RK. Phytoflavonoids: antiepileptics for the future. Int J Pharm Pharm Sci 2014;6:51–66.
   Google Scholar
• Campbell EL, Chebib M, Johnston GAR. The dietary flavonoids apigenin and (–)-epigallocatechin gallate enhance the positive modulation by diazepam of the activation by GABA of recombinant GABAA receptors. Biochem Pharmacol 2004;68:1631–8. doi: 10.1016/j.bcp.2004.07.022
   PubMed Web of Science ®Google Scholar
• Popova MS, Aniol VA, Lazareva NA, Stepanichev M, Yu Gulyaeva NV. Neurodegenerative changes in rat hippocampal fields during the development of pentylenetetrazole kindling. Neurosci Behav Physiol 2013;43:25–30.
   Google Scholar
• Taupin A. Apigenin and related compounds stimulate adult neurogenesis. Expert Opin Ther Pat 2009;19:523–7. doi: 10.1517/13543770902721279
   PubMed Web of Science ®Google Scholar
• Rose CR, Blum R, Kafitz KW, Kovalchuk Y., Konnerth A. From modulator to mediator: rapid effects of BDNF on ion channels. BioEssays 2004;26:1185–94. doi: 10.1002/bies.20118
   PubMed Web of Science ®Google Scholar
• Thoenen H. Neurotrophins and activity-dependent plasticity. Prog Brain Res 2000;128:183–91. doi: 10.1016/S0079-6123(00)28016-3
   PubMed Web of Science ®Google Scholar
• Elmér E, Kokaia M, Kokaia Z, Ferencz I, Lindvall O. Delayed kindling development after rapidly recurring seizures:relation to mossy fiber sprouting and neurotrophin, GAP-43 and dynorphin gene expression. Brain Res 1996;712:19–34. doi: 10.1016/0006-8993(95)01424-1
   PubMed Web of Science ®Google Scholar
• Kato H, Narita M, Miyatake M, Yajima Y, Suzuki T. Role of neuronal NR2B subunit-containing NMDA receptor-mediated Ca2+ influx and astrocytic activation in cultured mouse cortical neurons and astrocytes. Synapse 2006;2006(59):10–7. doi: 10.1002/syn.20213
   Google Scholar
• Zhu X, Dongc J, Shen K, Bai Y, Zhang Y, Lv X, et al. NMDA receptor NR2B subunits contribute to PTZ-kindling-induced hippocampal astrocytosis and oxidative stress. Brain Res Bull 2015;114:70–8. doi: 10.1016/j.brainresbull.2015.04.002
   PubMed Web of Science ®Google Scholar
• Giralt A, Friedman HC, Caneda-Ferrón B, Urbán N, Moreno E, Rubio N, et al. BDNF regulation under GFAP promoter provides engineered astrocytes as a new approach for long-term protection in Huntington’s disease. Gene Ther 2010;17:1294–308. doi: 10.1038/gt.2010.71
   PubMed Web of Science ®Google Scholar
• Heinrich C, Lähteinen S, Suzuki F, Anne-Marie L, Huber S, Häussler U, et al. Increase in BDNF-mediated TrkB signaling promotes epileptogenesis in a mouse model of mesial temporal lobe epilepsy. Neurobiol Dis 2011;42:35–47. doi: 10.1016/j.nbd.2011.01.001
   PubMed Web of Science ®Google Scholar
• Malhi SM, Huma JH, Hanif F, Ashraf N, Zubair F, Siddiqui BS, et al. Modulation of c-Fos and BDNF protein expression in pentylenetetrazole-kindled mice following the treatment with novel antiepileptic compound HHL-6. BioMed Res Int 2014. doi:10.1155/2014/876712.
   PubMed Web of Science ®Google Scholar
• Reibel S, Larmet F, Carnahan J, Marescaux C, Depaulis A. Endogenous control of hippocampal epileptogenesis: A molecular cascade involving brain-derived neurotrophic factor and neuropeptide Y. Epilepsia 2000;41:S127–S133. doi: 10.1111/j.1528-1157.2000.tb01571.x
   PubMed Web of Science ®Google Scholar
• Xu B, Michalski B, Racine RJ, Fahnestock M. The effects of brain derived neurotrophic factor (BDNF) administration on kindling induction Trk expression and seizure related morphological changes. Neuroscience 2004;126:521–31. doi: 10.1016/j.neuroscience.2004.03.044
   PubMed Web of Science ®Google Scholar
• Quesseveur G, David DJ, Gaillard MC, Pla P, Wu MV, Nguyen HT, et al. BDNF overexpression in mouse hippocampal astrocytes promotes local neurogenesis and elicits anxiolytic-like activities. Transl Psychiatry 2013;3:e253. doi:10.1038/tp.2013.30 doi: 10.1038/tp.2013.30
   PubMed Web of Science ®Google Scholar
• Pi X, Lee J, Li F, Rosenberg HC. Decreased expression of brain cAMP response element-binding protein gene following pentylenetetrazol seizure. Mol Brain Res 2004;127:60–7. doi: 10.1016/j.molbrainres.2004.05.006
   PubMedGoogle Scholar
• Mizuno M, Yamada K, Maekawa L, Saito K, Seishima M, Nabeshima T. CREB phosphorylation as a molecular marker of memory processing in the hippocampus for spatial learning. Behav Brain Res 2002;133:135–41. doi: 10.1016/S0166-4328(01)00470-3
   PubMed Web of Science ®Google Scholar
• Ortega-Martínez S. A new perspective on the role of the CREB family of transcription factors in memory consolidation via adult hippocampal neurogenesis. Front Mol Neurosci 2015;8:e1003310. doi: 10.3389/fnmol.2015.00046
   Web of Science ®Google Scholar
• Chen WF, Chang H, Huang LH, Lai MC, Yang CH, Wan TH, et al. Alterations in long-term seizure susceptibility and the complex of PSD-95 with NMDA receptor from animals previously exposed to perinatal hypoxia. Epilepsia 2006;47:288–96. doi: 10.1111/j.1528-1167.2006.00420.x
   PubMed Web of Science ®Google Scholar
• Nair A, Vaidya VA. Cyclic AMP response element binding protein and brain-derived neurotrophic factor: molecules that modulate our mood. J Biosci 2006;31:423–34. doi: 10.1007/BF02704114
   PubMed Web of Science ®Google Scholar
• Martin SJ, Grimwood PD, Morris RG. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 2000;23:649–711. doi: 10.1146/annurev.neuro.23.1.649
   PubMed Web of Science ®Google Scholar
• Yi LT, Li JM, Li YC, Pan Y, Xu Q, Kong LD. Antidepressant-like behavioral and neurochemical effects of the citrus-associated chemical apigenin. Life Sci 2008;82(13–14):741–51. doi: 10.1016/j.lfs.2008.01.007
   PubMed Web of Science ®Google Scholar
• Jiang DG, Jin SL, Li GY, Li QQ, Li ZR, Ma HX, et al. Serotonin regulates brain-derived neurotrophic factor expression in select brain regions during acute psychological stress. Neural Regen Res 2016;11:1471–9.
   PubMed Web of Science ®Google Scholar
• Deltheil T, Tanaka K, Reperant C, Hen R, David DJ, Gardier AM. Synergistic neurochemical and behavioural effects of acute intrahippocampal injection of brain derived neurotrophic factor and antidepressants in adult mice. Int J Neuropsychopharmacol 2009;12:905–15. doi: 10.1017/S1461145709000017
   PubMed Web of Science ®Google Scholar