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Original Research

Evaluation of the Effect of Hypericum triquetrifolium Turra on Memory Impairment Induced by Chronic Psychosocial Stress in Rats: Role of BDNF

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Pages 5299-5314 | Published online: 01 Dec 2020

References

  • De QuervainD, SchwabeL, RoozendaalB. Stress, glucocorticoids and memory: implications for treating fear-related disorders. Nat Rev Neurosci. 2017;18:7–19.27881856
  • RanabirS, ReetuK. Stress and hormones. Indian J Endocrinol Metab. 2011;15(1):18–22. doi:10.4103/2230-8210.7757321584161
  • SandiC. Stress, cognitive impairment and cell adhesion molecules. Nat Rev Neurosci. 2004;5(12):917–930. doi:10.1038/nrn155515550947
  • HuangRR, HuW, YinYY, WangYC, LiWP, LiWZ. Chronic restraint stress promotes learning and memory impairment due to enhanced neuronal endoplasmic reticulum stress in the frontal cortex and hippocampus in male mice. Int J Mol Med. 2015;35(2):553–559. doi:10.3892/ijmm.2014.202625482165
  • LiuD, WangZ, GaoZ, et al. Effects of curcumin on learning and memory deficits, BDNF, and ERK protein expression in rats exposed to chronic unpredictable stress. Behav Brain Res. 2014;271:116–121. doi:10.1016/j.bbr.2014.05.06824914461
  • XuY, PanJ, SunJ, et al. Inhibition of phosphodiesterase 2 reverses impaired cognition and neuronal remodeling caused by chronic stress. Neurobiol Aging. 2015;36(2):955–970. doi:10.1016/j.neurobiolaging.2014.08.02825442113
  • MoreiraPS, AlmeidaPR, Leite-AlmeidaH, SousaN, CostaP. Impact of chronic stress protocols in learning and memory in rodents: systematic review and meta-analysis. PLoS One. 2016;11(9):e0163245. doi:10.1371/journal.pone.016324527662580
  • ConradCD. A critical review of chronic stress effects on spatial learning and memory. Prog Neuropsychopharmacol Biol Psychiatry. 2010;34(5):742–755. doi:10.1016/j.pnpbp.2009.11.00319903505
  • FinsterwaldC, AlberiniCM. Stress and glucocorticoid receptor-dependent mechanisms in long-term memory: from adaptive responses to psychopathologies. Neurobiol Learn Mem. 2014;112:17–29. doi:10.1016/j.nlm.2013.09.01724113652
  • SandiC. Stress and cognition. Wiley Interdiscip Rev Cogn Sci. 2013;4(3):245–261.26304203
  • ConradCD, OrtizJB, JuddJM. Chronic stress and hippocampal dendritic complexity: methodological and functional considerations. Physiol Behav. 2017;178:66–81. doi:10.1016/j.physbeh.2016.11.01727887995
  • SchoenfeldTJ, McCauslandHC, MorrisHD, PadmanabanV, CameronHA. Stress and loss of adult neurogenesis differentially reduce hippocampal volume. Biol Psychiatry. 2017;82(12):914–923. doi:10.1016/j.biopsych.2017.05.01328629541
  • YagiS, GaleaLAM. Sex differences in hippocampal cognition and neurogenesis. Neuropsychopharmacology. 2019;44(1):200–213. doi:10.1038/s41386-018-0208-430214058
  • KimEJ, PellmanB, KimJJ. Stress effects on the hippocampus: a critical review. Learn Mem. 2015;22(9):411–416. doi:10.1101/lm.037291.11426286651
  • McEwenBS. Stress, sex, hippocampal plasticity: relevance to psychiatric disorders. Clin Neurosci Res. 2001;1(1):19–34. doi:10.1016/S1566-2772(00)00004-9
  • GaleaLAM, McEwenBS, TanapatP, DeakT, SpencerRL, DhabharFS. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience. 1997;81(3):689–697. doi:10.1016/S0306-4522(97)00233-99316021
  • ArboreliusL, OwensMJ, PlotskyPM, NemeroffCB. The role of corticotropin-releasing factor in depression and anxiety disorders. J Endocrinol. 1999;160(1):1–12. doi:10.1677/joe.0.16000019854171
  • HolsboerF. Stress, hypercortisolism and corticosteroid receptors in depression: implications for therapy. J Affect Disord. 2001;62(1–2):77–91. doi:10.1016/S0165-0327(00)00352-911172875
  • BouvierE, BrouillardF, MoletJ, et al. Nrf2-dependent persistent oxidative stress results in stress-induced vulnerability to depression. Mol Psychiatry. 2017;22(12):1701–1713. doi:10.1038/mp.2016.14427646262
  • WangY, KanH, YinY, et al. Protective effects of ginsenoside Rg1 on chronic restraint stress induced learning and memory impairments in male mice. Pharmacol Biochem Behav. 2014;120:73–81.24560910
  • SawyerK, CorsentinoE, Sachs-EricssonN, SteffensDC. Depression, hippocampal volume changes, and cognitive decline in a clinical sample of older depressed outpatients and non-depressed controls. Aging Ment Health. 2012;16(6):753–762. doi:10.1080/13607863.2012.67847822548411
  • VasicN, WalterH, HoseA, WolfRC. Gray matter reduction associated with psychopathology and cognitive dysfunction in unipolar depression: a voxel-based morphometry study. J Affect Disord. 2008;109(1–2):107–116. doi:10.1016/j.jad.2007.11.01118191459
  • EricksonKI, MillerDL, RoeckleinKA. The aging hippocampus: interactions between exercise, depression, and BDNF. Neuroscientist. 2012;18(1):82–97. doi:10.1177/107385841039705421531985
  • CzehB, LucassenPJ. What causes the hippocampal volume decrease in depression? Are neurogenesis, glial changes and apoptosis implicated? Eur Arch Psychiatry Clin Neurosci. 2007;257(5):250–260.17401728
  • BekinschteinP, CammarotaM, MedinaJH. BDNF and memory processing. Neuropharmacology. 2014;76(Pt):C:677–683. doi:10.1016/j.neuropharm.2013.04.024
  • AlonsoM, ViannaMR, DepinoAM, et al. BDNF-triggered events in the rat hippocampus are required for both short- and long-term memory formation. Hippocampus. 2002;12(4):551–560. doi:10.1002/hipo.1003512201640
  • KiprianovaI, FreimanTM, DesideratoS, et al. Brain-derived neurotrophic factor prevents neuronal death and glial activation after global ischemia in the rat. J Neurosci Res. 1999;56(1):21–27. doi:10.1002/(SICI)1097-4547(19990401)56:1<21::AID-JNR3>3.0.CO;2-Q10213471
  • ZaletelI, FilipovicD, PuskasN. Hippocampal BDNF in physiological conditions and social isolation. Rev Neurosci. 2017;28(6):675–692.28593903
  • Abdul-RazzakKK, AlzoubiKH, AbdoSA, HananehWM. High-dose vitamin C: does it exacerbate the effect of psychosocial stress on liver? Biochemical and histological study. Exp Toxicol Pathol. 2012;64(4):367–371. doi:10.1016/j.etp.2010.09.01121030226
  • AleisaAM, AlzoubiKH, GergesNZ, AlkadhiKA. Chronic psychosocial stress-induced impairment of hippocampal LTP: possible role of BDNF. Neurobiol Dis. 2006;22(3):453–462. doi:10.1016/j.nbd.2005.12.00516530419
  • AlzoubiKH, Abdul-RazzakKK, KhabourOF, Al-TuweiqGM, AlzubiMA, AlkadhiKA. Adverse effect of combination of chronic psychosocial stress and high fat diet on hippocampus-dependent memory in rats. Behav Brain Res. 2009;204(1):117–123. doi:10.1016/j.bbr.2009.05.02519482049
  • GergesNZ, AlzoubiKH, ParkCR, DiamondDM, AlkadhiKA. Adverse effect of the combination of hypothyroidism and chronic psychosocial stress on hippocampus-dependent memory in rats. Behav Brain Res. 2004;155(1):77–84. doi:10.1016/j.bbr.2004.04.00315325781
  • AlkadhiKA, AlzoubiKH, AleisaAM, TannerFL, NimerAS. Psychosocial stress-induced hypertension results from in vivo expression of long-term potentiation in rat sympathetic ganglia. Neurobiol Dis. 2005;20(3):849–857. doi:10.1016/j.nbd.2005.05.02016005635
  • Kukel’ovaD, BergaminiG, SigristH, SeifritzE, HengererB, PryceCR. Chronic social stress leads to reduced gustatory reward salience and effort valuation in mice. Front Behav Neurosci. 2018;12:134. doi:10.3389/fnbeh.2018.0013430057529
  • MohammadiHS, GoudarziI, LashkarboloukiT, AbrariK, Elahdadi SalmaniM. Chronic administration of quercetin prevent spatial learning and memory deficits provoked by chronic stress in rats. Behav Brain Res. 2014;270:196–205. doi:10.1016/j.bbr.2014.05.01524844750
  • NgQX, VenkatanarayananN, HoCY. Clinical use of Hypericum perforatum (St John’s wort) in depression: a meta-analysis. J Affect Disord. 2017;210:211–221. doi:10.1016/j.jad.2016.12.04828064110
  • KumarV, SinghPN, MuruganandamAV, BhattacharyaSK. Effect of Indian Hypericum perforatum Linn on animal models of cognitive dysfunction. J Ethnopharmacol. 2000;72(1–2):119–128. doi:10.1016/S0378-8741(00)00216-610967462
  • KlusaV, GermaneS, NoldnerM, ChatterjeeSS. Hypericum extract and hyperforin: memory-enhancing properties in rodents. Pharmacopsychiatry. 2001;34(Suppl 1):S61–69. doi:10.1055/s-2001-1545111518079
  • GonulalanEM, NemutluE, BayazeidO, KocakE, YalcinFN, DemirezerLO. Metabolomics and proteomics profiles of some medicinal plants and correlation with BDNF activity. Phytomedicine. 2019;152920.30979692
  • GryzlakBM, WallaceRB, ZimmermanMB, NislyNL. National surveillance of herbal dietary supplement exposures: the poison control center experience. Pharmacoepidemiol Drug Saf. 2007;16(9):947–957. doi:10.1002/pds.144517613175
  • RychlikR, SiedentopH, von den DrieschV, KasperS. General practice research study of St. Johns wort extract WS 5572. Normally 600 mg per day is enough. MMW Fortschr Med. 2001;143(47):48.
  • LecrubierY, ClercG, DidiR, KieserM. Efficacy of St. John’s wort extract WS 5570 in major depression: a double-blind, placebo-controlled trial. Am J Psychiatry. 2002;159(8):1361–1366. doi:10.1176/appi.ajp.159.8.136112153829
  • ValvassoriSS, BorgesC, BavarescoDV, et al. Hypericum perforatum chronic treatment affects cognitive parameters and brain neurotrophic factor levels. Braz J Psychiatry. 2018;40(4):367–375. doi:10.1590/1516-4446-2017-227130110089
  • AleisaAM. Cytological and biochemical effects of St. John’s wort supplement (a complex mixture of St. John’s wort, Rosemary and Spirulina) on somatic and germ cells of Swiss Albino mice. Int J Environ Res Public Health. 2008;5(5):408–417. doi:10.3390/ijerph505040819151436
  • Al-EisawiDM. Field Guide to Wild Flowers of Jordan and Neighbouring Countries. Amman, Jordan: Jordan Press Founation, Al-Rai; 1998.
  • NurkNM, CrockettSL. Morphological and phytochemical diversity among hypericum species of the mediterranean basin. Med Aromat Plant Sci Biotechnol. 2011;5(SpecialIssue 1):14–28.22662020
  • AlaliFQ, TawahaK, El-ElimatT, et al. Antioxidant activity and total phenolic content of aqueous and methanolic extracts of Jordanian plants: an ICBG project. Nat Prod Res. 2007;21(12):1121–1131. doi:10.1080/1478641070159028517852749
  • TawahaK, AlaliFQ, GharaibehM, MohammadM, El-ElimatT. Antioxidant activity and total phenolic content of selected Jordanian plant species. Food Chem. 2007;104(4):1372–1378. doi:10.1016/j.foodchem.2007.01.064
  • MizunoM, YamadaK, HeJ, NakajimaA, NabeshimaT. Involvement of BDNF receptor TrkB in spatial memory formation. Learn Mem. 2003;10(2):108–115. doi:10.1101/lm.5600312663749
  • DuruB. Isolation of a Bioactive Compound Hypericin from a Medicinal Plant Hypericum perforatum L. Using Basic Chromatography Methods. Department of Chemistry, The Middle East Technical University; 2003.
  • Office of Laboratory Animal Welfare. AR. The Institutional Animal Care and Use Committee Guidebook. 2nd edition. ARENA and OLAW; 2002.
  • AlzoubiKH, Abdul-RazzakKK, KhabourOF, Al-TuweiqGM, AlzubiMA, AlkadhiKA. Caffeine prevents cognitive impairment induced by chronic psychosocial stress and/or high fat-high carbohydrate diet. Behav Brain Res. 2013;237:7–14. doi:10.1016/j.bbr.2012.09.01823000531
  • AlzoubiKH, SrivareeratM, AleisaAM, AlkadhiKA. Chronic caffeine treatment prevents stress-induced LTP impairment: the critical role of phosphorylated CaMKII and BDNF. J Mol Neurosci. 2013;49(1):11–20. doi:10.1007/s12031-012-9836-z22706686
  • SrivareeratM, TranTT, AlzoubiKH, AlkadhiKA. Chronic psychosocial stress exacerbates impairment of cognition and long-term potentiation in beta-amyloid rat model of Alzheimer’s disease. Biol Psychiatry. 2009;65(11):918–926. doi:10.1016/j.biopsych.2008.08.02118849021
  • ExarchouV, FiamegosYC, van BeekTA, NanosC, VervoortJ. Hyphenated chromatographic techniques for the rapid screening and identification of antioxidants in methanolic extracts of pharmaceutically used plants. J Chromatogr A. 2006;1112(1):293–302. doi:10.1016/j.chroma.2005.11.07716359690
  • AbdullahY, SchneiderB, PetersenM. Occurrence of rosmarinic acid, chlorogenic acid and rutin in Marantaceae species. Phytochem Lett. 2008;1(4):199–203.
  • TatsisEC, ExarchouV, TroganisAN, GerothanassisIP. 1H NMR determination of hypericin and pseudohypericin in complex natural mixtures by the use of strongly deshielded OH groups. Anal Chim Acta. 2008;607(2):219–226. doi:10.1016/j.aca.2007.11.04018190811
  • MorrisRG, GarrudP, RawlinsJN, O’KeefeJ. Place navigation impaired in rats with hippocampal lesions. Nature. 1982;297(5868):681–683. doi:10.1038/297681a07088155
  • StewartS, CacucciF, LeverC. Which memory task for my mouse? A systematic review of spatial memory performance in the Tg2576 Alzheimer’s mouse model. J Alzheimers Dis. 2011;26(1):105–126. doi:10.3233/JAD-2011-101827
  • LicinioJ, WongM. Brain-derived neurotrophic factor (BDNF) in stress and affective disorders. Mol Psychiatry. 2002;7(6):519.12140770
  • SmithMA, MakinoS, KimSY, KvetnanskyR. Stress increases brain-derived neurotropic factor messenger ribonucleic acid in the hypothalamus and pituitary. Endocrinology. 1995;136(9):3743–3750. doi:10.1210/endo.136.9.76490807649080
  • MarosiK, MattsonMP. BDNF mediates adaptive brain and body responses to energetic challenges. Trends Endocrinol Metab. 2014;25(2):89–98. doi:10.1016/j.tem.2013.10.00624361004
  • BulyginaVV, ShishkinaGT, BerezovaIV, DygaloNN. BDNF protein expression in the hippocampus following exposure of rats to forced swimming stress. Dokl Biol Sci. 2011;437(1):82–84. doi:10.1134/S001249661102011621562951
  • FilhoCB, JesseCR, DonatoF, et al. Chronic unpredictable mild stress decreases BDNF and NGF levels and Na(+), K(+)-ATPase activity in the hippocampus and prefrontal cortex of mice: antidepressant effect of chrysin. Neuroscience. 2015;289:367–680. doi:10.1016/j.neuroscience.2014.12.04825592430
  • McEwenBS. Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators. Eur J Pharmacol. 2008;583(2–3):174–185. doi:10.1016/j.ejphar.2007.11.07118282566
  • AmriH, DrieuK, PapadopoulosV. Ex vivo regulation of adrenal cortical cell steroid and protein synthesis, in response to adrenocorticotropic hormone stimulation, by the Ginkgo biloba extract EGb 761 and isolated ginkgolide B. Endocrinology. 1997;138(12):5415–5426. doi:10.1210/endo.138.12.56049389527
  • SchoenfeldTJ, GouldE. Stress, stress hormones, and adult neurogenesis. Exp Neurol. 2012;233(1):12–21. doi:10.1016/j.expneurol.2011.01.00821281629
  • BurgessN, MaguireEA, O’KeefeJ. The human hippocampus and spatial and episodic memory. Neuron. 2002;35(4):625–641.12194864
  • KosakiY, LinTC, HorneMR, PearceJM, GilroyKE. The role of the hippocampus in passive and active spatial learning. Hippocampus. 2014;24(12):1633–1652. doi:10.1002/hipo.2234325131441
  • ArbelI, KadarT, SilbermannM, LevyA. The effects of long-term corticosterone administration on hippocampal morphology and cognitive performance of middle-aged rats. Brain Res. 1994;657(1–2):227–235.7820622
  • ConradCD, GaleaLA, KurodaY, McEwenBS. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav Neurosci. 1996;110(6):1321–1334. doi:10.1037/0735-7044.110.6.13218986335
  • DachirS, KadarT, RobinzonB, LevyA. Cognitive deficits induced in young rats by long-term corticosterone administration. Behav Neural Biol. 1993;60(2):103–109. doi:10.1016/0163-1047(93)90173-F8117235
  • StillmanMJ, Shukitt-HaleB, LevyA, LiebermanHR. Spatial memory under acute cold and restraint stress. Physiol Behav. 1998;64(5):605–609. doi:10.1016/S0031-9384(98)00091-29817570
  • StickgoldR, WalkerMP. Memory consolidation and reconsolidation: what is the role of sleep? Trends Neurosci. 2005;28(8):408–415. doi:10.1016/j.tins.2005.06.00415979164
  • BornJ, WilhelmI. System consolidation of memory during sleep. Psychol Res. 2012;76(2):192–203. doi:10.1007/s00426-011-0335-621541757
  • DudaiY. The restless engram: consolidations never end. Annu Rev Neurosci. 2012;35(1):227–247. doi:10.1146/annurev-neuro-062111-15050022443508
  • McGaughJL. Memory – a century of consolidation. Science. 2000;287(5451):248–251. doi:10.1126/science.287.5451.24810634773
  • NaderK. Memory traces unbound. Trends Neurosci. 2003;26(2):65–72. doi:10.1016/S0166-2236(02)00042-512536129
  • WamsleyEJ, StickgoldR. Memory, sleep and dreaming: experiencing consolidation. Sleep Med Clin. 2011;6(1):97–108. doi:10.1016/j.jsmc.2010.12.00821516215
  • DupretD, O’NeillJ, Pleydell-BouverieB, CsicsvariJ. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nat Neurosci. 2010;13(8):995–1002. doi:10.1038/nn.259920639874
  • TamminenJ, PayneJD, StickgoldR, WamsleyEJ, GaskellMG. Sleep spindle activity is associated with the integration of new memories and existing knowledge. J Neurosci. 2010;30(43):14356–14360. doi:10.1523/JNEUROSCI.3028-10.201020980591
  • DumayN, GaskellMG. Sleep-associated changes in the mental representation of spoken words. Psychol Sci. 2007;18(1):35–39. doi:10.1111/j.1467-9280.2007.01845.x17362375
  • PayneJD, SchacterDL, PropperRE, et al. The role of sleep in false memory formation. Neurobiol Learn Mem. 2009;92(3):327–334. doi:10.1016/j.nlm.2009.03.00719348959
  • WagnerU, GaisS, HaiderH, VerlegerR, BornJ. Sleep inspires insight. Nature. 2004;427(6972):352–355. doi:10.1038/nature0222314737168
  • ZhangY, GruberR. Can slow-wave sleep enhancement improve memory? A review of current approaches and cognitive outcomes. Yale J Biol Med. 2019;92(1):63–80.30923474
  • SmithC. Sleep states and memory processes in humans: procedural versus declarative memory systems. Sleep Med Rev. 2001;5(6):491–506. doi:10.1053/smrv.2001.016412531156
  • SkaggsWE, McNaughtonBL. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science. 1996;271(5257):1870–1873. doi:10.1126/science.271.5257.18708596957
  • KudrimotiHS, BarnesCA, McNaughtonBL. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci. 1999;19(10):4090–4101. doi:10.1523/JNEUROSCI.19-10-04090.199910234037
  • PeigneuxP, LaureysS, FuchsS, et al. Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron. 2004;44(3):535–545. doi:10.1016/j.neuron.2004.10.00715504332
  • SutherlandGR, McNaughtonB. Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Curr Opin Neurobiol. 2000;10(2):180–186. doi:10.1016/S0959-4388(00)00079-910753801
  • StickgoldR. EMDR: a putative neurobiological mechanism of action. J Clin Psychol. 2002;58(1):61–75. doi:10.1002/jclp.112911748597
  • DiekelmannS, BornJ. The memory function of sleep. Nat Rev Neurosci. 2010;11(2):114–126. doi:10.1038/nrn276220046194
  • PhillipsC. Brain-derived neurotrophic factor, depression, and physical activity: making the neuroplastic connection. Neural Plast. 2017;2017:7260130. doi:10.1155/2017/726013028928987
  • TorderaRM, Garcia-GarciaAL, ElizaldeN, et al. Chronic stress and impaired glutamate function elicit a depressive-like phenotype and common changes in gene expression in the mouse frontal cortex. Eur Neuropsychopharmacol. 2011;21(1):23–32. doi:10.1016/j.euroneuro.2010.06.01620937555
  • VasquezCE, RienerR, ReynoldsE, BrittonGB. NMDA receptor dysregulation in chronic state: a possible mechanism underlying depression with BDNF downregulation. Neurochem Int. 2014;79:88–97. doi:10.1016/j.neuint.2014.09.00725277075
  • WangC, GuoJ, GuoR. Effect of XingPiJieYu decoction on spatial learning and memory and cAMP-PKA-CREB-BDNF pathway in rat model of depression through chronic unpredictable stress. BMC Complement Altern Med. 2017;17(1):73. doi:10.1186/s12906-016-1543-928118829
  • EnogieruAB, HaylettW, HissDC, BardienS, EkpoOE. Rutin as a potent antioxidant: implications for neurodegenerative disorders. Oxid Med Cell Longev. 2018;2018:1–17. doi:10.1155/2018/6241017
  • OrcicDZ, Mimica-DukicNM, FranciskovicMM, PetrovicSS, JovinED. Antioxidant activity relationship of phenolic compounds in Hypericum perforatum L. Chem Cent J. 2011;5:34. doi:10.1186/1752-153X-5-34.21702979
  • ÇirakC, RadusieneJ, JanulisV, IvanauskasL, CamasN, AyanA. Phenolic constituents of Hypericum triquetrifolium Turra (Guttiferae) growing in Turkey: variation among populations and plant parts. Turk J Biol. 2011;35:449–456.
  • Nassiri-AslM, NaserpourT, AbbasiE, et al. Effects of rutin on oxidative stress in mice with kainic acid-induced seizure. J Integr Med. 2013;11(5):337–342. doi:10.3736/jintegrmed201304224063781
  • SivananthamB, KrishnanU, RajendiranV. Amelioration of oxidative stress in differentiated neuronal cells by rutin regulated by a concentration switch. Biomed Pharmacother. 2018;108:15–26. doi:10.1016/j.biopha.2018.09.02130212708
  • SongK, NaJY, KimS, KwonJ. Rutin upregulates neurotrophic factors resulting in attenuation of ethanol-induced oxidative stress in HT22 hippocampal neuronal cells. J Sci Food Agric. 2014;95.23633396
  • AlaliF, TawahaK, El-ElimatT. Determination of hypericin content in Hypericum triquetrifolium Turra (Hypericaceae) growing wild in Jordan. Nat Prod Res. 2004;18(2):147–151. doi:10.1080/1478641031000160804614984088
  • GarciaI, BallestaS, GilaberteY, RezustaA, PascualÁ. Antimicrobial photodynamic activity of hypericin against methicillin-susceptible and resistant Staphylococcus aureus biofilms. Future Microbiol. 2015;10(3):347–356. doi:10.2217/fmb.14.11425812458
  • KariotiA, BiliaAR. Hypericins as potential leads for new therapeutics. Int J Mol Sci. 2010;11(2):562–594. doi:10.3390/ijms1102056220386655
  • BannermanDM, GoodMA, ButcherSP, RamsayM, MorrisRG. Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature. 1995;378(6553):182–186. doi:10.1038/378182a07477320
  • TawahaK, SadiR, Qa’danF, MatalkaKZ, NahrstedtA. A bioactive prodelphinidin from Mangifera indica leaf extract. Z Naturforsch C J Biosci. 2010;65(5–6):322–326. doi:10.1515/znc-2010-5-60320653233
  • KumarV, MdzinarishviliA, KiewertC, et al. NMDA receptor-antagonistic properties of hyperforin, a constituent of St. John’s Wort. J Pharmacol Sci. 2006;102(1):47–54. doi:10.1254/jphs.FP006037816936454
  • PalmerGC. Neuroprotection by NMDA receptor antagonists in a variety of neuropathologies. Curr Drug Targets. 2001;2(3):241–271. doi:10.2174/138945001334833511554551
  • MenniniT, GobbiM. The antidepressant mechanism of Hypericum perforatum. Life Sci. 2004;75(9):1021–1027. doi:10.1016/j.lfs.2004.04.00515207650
  • WeiS, JiXW, WuCL, et al. Resident intruder paradigm-induced aggression relieves depressive-like behaviors in male rats subjected to chronic mild stress. Med Sci Monit. 2014;20:945–952. doi:10.12659/MSM.89020024911067
  • DumanRS, MonteggiaLM. A neurotrophic model for stress-related mood disorders. Biol Psychiatry. 2006;59(12):1116–1127. doi:10.1016/j.biopsych.2006.02.01316631126
  • Russo-NeustadtA, HaT, RamirezR, KesslakJP. Physical activity-antidepressant treatment combination: impact on brain-derived neurotrophic factor and behavior in an animal model. Behav Brain Res. 2001;120(1):87–95. doi:10.1016/S0166-4328(00)00364-811173088
  • ZhangR, PengZ, WangH, et al. Gastrodin ameliorates depressive-like behaviors and up-regulates the expression of BDNF in the hippocampus and hippocampal-derived astrocyte of rats. Neurochem Res. 2014;39(1):172–179. doi:10.1007/s11064-013-1203-024293261
  • AutryAE, MonteggiaLM. Brain-derived neurotrophic factor and neuropsychiatric disorders. Pharmacol Rev. 2012;64(2):238–258. doi:10.1124/pr.111.00510822407616
  • ConboyL, TanrikutC, ZoladzPR, et al. The antidepressant agomelatine blocks the adverse effects of stress on memory and enables spatial learning to rapidly increase neural cell adhesion molecule (NCAM) expression in the hippocampus of rats. Int J Neuropsychopharmacol. 2009;12(3):329–341. doi:10.1017/S146114570800925518706130
  • Yadollah-DamavandiS, Chavoshi-NejadM, JangholiE, et al. Topical Hypericum perforatum improves tissue regeneration in full-thickness excisional wounds in diabetic rat model. Evid Based Complement Alternat Med. 2015;2015:245328. doi:10.1155/2015/24532826417372
  • KlemowKM, BartlowA, CrawfordJ, KocherN, ShahJ, RitsickM. Medical attributes of St. John’s wort (Hypericum perforatum) In: BenzieIFF, Wachtel-GalorS, editors. Herbal Medicine: Biomolecular and Clinical Aspects. Boca Raton (FL);2011.
  • WhiskeyE, WernekeU, TaylorD. A systematic review and meta-analysis of Hypericum perforatum in depression: a comprehensive clinical review. Int Clin Psychopharmacol. 2001;16(5):239–252. doi:10.1097/00004850-200109000-0000111552767
  • SiepmannM, KrauseS, JoraschkyP, Muck-WeymannM, KirchW. The effects of St John’s wort extract on heart rate variability, cognitive function and quantitative EEG: a comparison with amitriptyline and placebo in healthy men. Br J Clin Pharmacol. 2002;54(3):277–282. doi:10.1046/j.1365-2125.2002.01658.x12236848