Therapeutic effects of saffron extract on different memory types, anxiety, and hippocampal BDNF and TNF-α gene expressions in sub-chronically stressed rats

References

• García-Iglesias BB, Mendoza-Garrido ME, Gutiérrez-Ospina G, Rangel-Barajas C, Noyola-Díaz M, Terrón JA, et al. Sensitization of restraint-induced corticosterone secretion after chronic restraint in rats: involvement of 5-HT₇ receptors. Neuropharmacology. 2013;71:216–227.
   PubMed Web of Science ®Google Scholar
• Woo H, Hong CJ, Jung S, Choe S, Yu S-W, et al. Chronic restraint stress induces hippocampal memory deficits by impairing insulin signaling. Mol Brain. 2018;11:1–13. 37.
   PubMed Web of Science ®Google Scholar
• Bowman RE, Kelly R. Chronically stressed female rats show increased anxiety but no behavioral alterations in object recognition or placement memory: a preliminary examination. Stress. 2012;15:524–532.
   PubMed Web of Science ®Google Scholar
• Nawaz A, Batool Z, Shazad S, et al. Physical enrichment enhances memory function by regulating stress hormone and brain acetylcholinesterase activity in rats exposed to restraint stress. Life Sci. 2018;207:42–49.
   PubMed Web of Science ®Google Scholar
• Şahin TD, Karson A, Balcı F, et al. TNF-alpha inhibition prevents cognitive decline and maintains hippocampal BDNF levels in the unpredictable chronic mild stress rat model of depression. Behav Brain Res. 2015;292:233–240.
   PubMed Web of Science ®Google Scholar
• Amin SN, El-Aidi AA, Ali MM, Attia YM, Rashed LA, et al. Modification of hippocampal markers of synaptic plasticity by memantine in animal models of acute and repeated restraint stress: implications for memory and behavior. Neuromolecular Med. 2015;17:121–136.
   PubMed Web of Science ®Google Scholar
• Pitsikas N, Tarantilis PA. Crocins, the active constituents of Crocus sativus L., counteracted apomorphine-induced performance deficits in the novel object recognition task, but not novel object location task, in rats. Neurosci Lett. 2017;644:37–42.
   PubMed Web of Science ®Google Scholar
• Pitsikas N. The effect of Crocus sativus L. and Its constituents on memory: basic studies and clinical applications. Evid Based Complement Alternat Med. 2015;2015:1–7. 926284.
   Web of Science ®Google Scholar
• Khazdair MR, Anaeigoudari A, Hashemzehi M, Mohebbati R, et al. Neuroprotective potency of some spice herbs, a literature review. J Tradit Complement Med. 2019;9:98–105.
   PubMedGoogle Scholar
• Pitsikas N, Sakellaridis N. Crocus sativus L. extracts antagonize memory impairments in different behavioural tasks in the rat. Behav Brain Res. 2006;173:112–115.
   PubMed Web of Science ®Google Scholar
• Pitsikas N, Zisopoulou S, Tarantilis PA, Kanakis C, Polissiou M, Sakellaridis N, et al. Effects of the active constituents of Crocus sativus L., crocins on recognition and spatial rats’ memory. Behav Brain Res. 2007;183:141–146.
   PubMed Web of Science ®Google Scholar
• Elizabeth A, Adegbuyi A, Olusegun A, Benneth B-A, Anthony E, Abayomi A, Solomon U, et al. Morin hydrate attenuates chronic stress-induced memory impairment and degeneration of hippocampal subfields in mice: The role of oxidative, nitrergic and neuroinflammatory pathways. Metab Brain Dis. 2020;35:1145–1156.
   PubMed Web of Science ®Google Scholar
• Wood GE, Young LT, Reagan LP, McEwen BS, et al. Acute and chronic restraint stress alter the incidence of social conflict in male rats. Horm Behav. 2003;43:205–213.
   PubMed Web of Science ®Google Scholar
• Patchev VK, Patchev AV. Stress. Dialogues Clin Neurosci. 2006;8:417–432.
   PubMedGoogle Scholar
• Ranjbar H, Radahmadi M, Alaei H, Reisi P, Karimi S, et al. The effect of basolateral amygdala nucleus lesion on memory under acute,mid and chronic stress in male rats. Turkish J Med Sci. 2016;46:1915–1925.
   PubMed Web of Science ®Google Scholar
• Ranjbar H, Radahmadi M, Reisi P, et al. Effects of electrical lesion of basolateral amygdala nucleus on rat anxiety-like behaviour under acute, sub-chronic, and chronic stresses. Clin Exp Pharmacol Physiol. 2017;44:470–479.
   PubMed Web of Science ®Google Scholar
• Barbato C, Giacovazzo G, Albiero F, Scardigli R, Scopa C, Ciotti MT, et al. Cognitive decline and modulation of Alzheimer’s disease-Related genes after inhibition of MicroRNA-101 in mouse hippocampal neurons. Mol Neurobiol. 2020;57:3183–3194.
   PubMed Web of Science ®Google Scholar
• Ghorbanpour AM, Saboor M, Panahizadeh R, Saadati H, Dadkhah M, et al. Combined effects of royal jelly and environmental enrichment against stress-induced cognitive and behavioral alterations in male rats: behavioral and molecular studies. Nutr Neurosci. 2021;24:1–12.
   PubMedGoogle Scholar
• Gould TD, Dao DT, Kovacsics CE. The Open Field Test BT - Mood and Anxiety Related Phenotypes in Mice: Characterization Using Behavioral Tests. In: Gould TD, editor. Totowa, NJ: Humana Press; 2009. p. 1–20. Available from: https://doi.org/https://doi.org/10.1007/978-1-60761-303-9_1.
   Google Scholar
• Radahmadi M, Alaei H, Sharifi MR, Hosseini N, et al. Effects of different timing of stress on corticosterone, BDNF and memory in male rats. Physiol Behav. 2015;139:459–467.
   PubMed Web of Science ®Google Scholar
• Ainge JA, Heron-Maxwell C, Theofilas P, Wright P, de Hoz L, Wood ER, et al. The role of the hippocampus in object recognition in rats: examination of the influence of task parameters and lesion size. Behav Brain Res. 2006;167:183–195.
   PubMed Web of Science ®Google Scholar
• Hughes RN. Neotic preferences in laboratory rodents: issues, assessment and substrates. Neurosci Biobehav Rev. 2007;31:441–464.
   PubMed Web of Science ®Google Scholar
• Workman JL, Fonken LK, Gusfa J, Kassouf KM, Nelson RJ, et al. Post-weaning environmental enrichment alters affective responses and interacts with behavioral testing to alter nNOS immunoreactivity. Pharmacol Biochem Behav. 2011;100:25–32.
   PubMed Web of Science ®Google Scholar
• Hosseinzadeh H, Noraei NB. Anxiolytic and hypnotic effect of Crocus sativus aqueous extract and its constituents, crocin and safranal, in mice. Phytother Res. 2009;23:768–774.
   PubMed Web of Science ®Google Scholar
• Eidelkhani N, Radahmadi M, Kazemi M, et al. Effects of doxepin on brain-derived neurotrophic factor, tumor necrosis factor alpha, mitogen-activated protein kinase 14, and AKT1 genes expression in rat hippocampus. Adv Biomed Res. 2015;4:1–5. 203.
   PubMedGoogle Scholar
• Wang Q, Yu K, Wang J, Lin H, Wu Y, Wang W, et al. Predator stress-induced persistent emotional arousal is associated with alterations of plasma corticosterone and hippocampal steroid receptors in rat. Behav Brain Res. 2012;230:167–174.
   PubMed Web of Science ®Google Scholar
• Gray M, Bingham B, Viau V. A comparison of two repeated restraint stress paradigms on hypothalamic-pituitary-adrenal axis habituation, gonadal status and central neuropeptide expression in adult male rats. J Neuroendocrinol. 2010;22:92–101.
   PubMed Web of Science ®Google Scholar
• Barnum CJ, Blandino PJ, Deak T. Adaptation in the corticosterone and hyperthermic responses to stress following repeated stressor exposure. J Neuroendocrinol. 2007;19:632–642.
   PubMed Web of Science ®Google Scholar
• Gądek-Michalska A, Spyrka J, Rachwalska P, Tadeusz J, Bugajski J, et al. Influence of chronic stress on brain corticosteroid receptors and HPA axis activity. Pharmacol Rep. 2013;65:1163–1175.
   PubMed Web of Science ®Google Scholar
• Imperato A, Puglisi-Allegra S, Casolini P, Angelucci L, et al. Changes in brain dopamine and acetylcholine release during and following stress are independent of the pituitary-adrenocortical axis. Brain Res. 1991;538:111–117.
   PubMed Web of Science ®Google Scholar
• Bowman RE, Micik R, Gautreaux C, Fernandez L, Luine VN. Sex-dependent changes in anxiety, memory, and monoamines following one week of stress. Physiol Behav. 2009;97:21–29.
   PubMed Web of Science ®Google Scholar
• Schwabe L, Joëls M, Roozendaal B, Wolf OT, Oitzl MS, et al. Stress effects on memory: an update and integration. Neurosci Biobehav Rev. 2012;36:1740–1749.
   PubMed Web of Science ®Google Scholar
• Yang C, Tang J, Liang X, Qi Y, Luo Y, Xie Y, et al. Anti-LINGO-1 antibody treatment improves chronic stress-induced spatial memory impairments and oligodendrocyte loss in the hippocampus. Behav Brain Res. 2020;393: 112765.
   Google Scholar
• Vodička M, Vavřínová A, Mikulecká A, Zicha J, Behuliak M, et al. Hyper-reactivity of HPA axis in fischer 344 rats is associated with impaired cardiovascular and behavioral adaptation to repeated restraint stress. Stress. 2020;23:667–677.
   PubMed Web of Science ®Google Scholar
• Bhakta A, Gavini K, Yang E, Lyman-Henley L, Parameshwaran K, et al. Chronic traumatic stress impairs memory in mice: potential roles of acetylcholine, neuroinflammation and corticotropin releasing factor expression in the hippocampus. Behav Brain Res. 2017;335:32–40.
   PubMed Web of Science ®Google Scholar
• Lakshminarasimhan H, Chattarji S. Stress leads to contrasting effects on the levels of brain derived neurotrophic factor in the hippocampus and amygdala. PLoS One. 2012;7:1–6. e30481.
   Web of Science ®Google Scholar
• Filho CB, Jesse CR, Donato F, Giacomeli R, Del Fabbro L, da Silva Antunes M, 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;289:367–380.
   PubMed Web of Science ®Google Scholar
• Bennett MR, Lagopoulos J. Stress and trauma: BDNF control of dendritic-spine formation and regression. Prog Neurobiol. 2014;112:80–99.
   PubMed Web of Science ®Google Scholar
• Ettehadi H, Mojabi SN, Ranjbaran M, et al. Aqueous extract of saffron (Crocus sativus) increases brain dopamine and glutamate concentrations in rats. 2013.
   Google Scholar
• Zhao Y, Xi G. Safranal-promoted differentiation and survival of dopaminergic neurons in an animal model of Parkinson’s disease. Pharm Biol. 2018;56:450–454.
   PubMed Web of Science ®Google Scholar
• Lin S, Li Q, Jiang S, Xu Z, Jiang Y, Liu L, et al. Crocetin ameliorates chronic restraint stress-induced depression-like behaviors in mice by regulating MEK/ERK pathways and gut microbiota. J Ethnopharmacol. 2021;268: 113608.
   PubMed Web of Science ®Google Scholar
• Yuan Y, Shan X, Men W, Zhai H, Qiao X, Geng L, Li C, et al. The effect of crocin on memory, hippocampal acetylcholine level, and apoptosis in a rat model of cerebral ischemia. Biomed Pharmacother. 2020;130:1–6. 110543.
   Web of Science ®Google Scholar
• D’Onofrio G, Nabavi SM, Sancarlo D, et al. Crocus sativus L. (saffron) in Alzheimer’s disease treatment: bioactive effects on cognitive impairment. Curr Neuropharmacol. 2021;19.
   PubMed Web of Science ®Google Scholar
• Berger F, Hensel A, Nieber K. Saffron extract and trans-crocetin inhibit glutamatergic synaptic transmission in rat cortical brain slices. Neuroscience. 2011;180:238–247.
   PubMed Web of Science ®Google Scholar
• Myhrer T. Neurotransmitter systems involved in learning and memory in the rat: a meta-analysis based on studies of four behavioral tasks. Brain Res Brain Res Rev. 2003;41:268–287.
   PubMed Web of Science ®Google Scholar
• Antunes M, Biala G. The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn Process [Internet. 2012;13:93–110. doi:https://doi.org/10.1007/s10339-011-0430-z.
   PubMed Web of Science ®Google Scholar
• Pitsikas N, Boultadakis A, Georgiadou G, Tarantilis PA, Sakellaridis N, et al. Effects of the active constituents of Crocus sativus L., crocins, in an animal model of anxiety. Phytomedicine. 2008;15:1135–1139.
   PubMed Web of Science ®Google Scholar
• Pitsikas N, Tarantilis PA. The GABA(A)-benzodiazepine receptor antagonist flumazenil abolishes the anxiolytic effects of the active constituents of Crocus sativus L. Crocins in rats. Molecules. 2020;25:1–9. 5647.
   Web of Science ®Google Scholar
• Hosseinzadeh H, Jahanian Z. Effect of Crocus sativus L. (saffron) stigma and its constituents, crocin and safranal, on morphine withdrawal syndrome in mice. Phytother Res. 2010;24:726–730.
   PubMed Web of Science ®Google Scholar
• Mohammadzadeh L, Hosseinzadeh H, Abnous K, Razavi BM. Neuroprotective potential of crocin against malathion-induced motor deficit and neurochemical alterations in rats. Environ Sci Pollut Res Int. 2018;25:4904–4914.
   PubMed Web of Science ®Google Scholar
• Zhang L, Previn R, Lu L, Liao R-F, Jin Y, Wang R-K, et al. Crocin, a natural product attenuates lipopolysaccharide-induced anxiety and depressive-like behaviors through suppressing NF-kB and NLRP3 signaling pathway. Brain Res Bull. 2018;142:352–359.
   PubMed Web of Science ®Google Scholar
• Halataei B-a-S, Khosravi M, Arbabian S, Sahraei H, Golmanesh L, Zardooz H, et al. Saffron (Crocus sativus) aqueous extract and its constituent crocin reduces stress-induced anorexia in mice. Phytother Res. 2011;25:1833–1838.
   PubMed Web of Science ®Google Scholar
• Asalgoo S., Tat M, Sahraei H, Pirzad Jahromi G. The Psychoactive Agent Crocin Can Regulate Hypothalamic-Pituitary-Adrenal Axis Activity. Front Neurosci. 2017;11:1–10. 668.
   PubMed Web of Science ®Google Scholar
• Ghalandari-Shamami M, Nourizade S, Barati M, Yousefi B, Pashayi M, Ali Vafaei A, et al. Exercise and crocin prevent adolescent-stress induced impairment of spatial navigation and dendritic retraction in the hippocampal CA3 area in adult male rats. Brain Res. 2021;1754: 147274.
   Google Scholar
• Shafahi M, Vaezi G, Shajiee H, Sharafi S, Khaksari M, et al. Crocin inhibits apoptosis and astrogliosis of hippocampus neurons against methamphetamine neurotoxicity via antioxidant and anti-inflammatory mechanisms. Neurochem Res. 2018;43:2252–2259.
   PubMed Web of Science ®Google Scholar
• Ghadrdoost B, Vafaei AA, Rashidy-Pour A, Hajisoltani R, Bandegi AR, Motamedi F, et al. Protective effects of saffron extract and its active constituent crocin against oxidative stress and spatial learning and memory deficits induced by chronic stress in rats. Eur J Pharmacol. 2011;667:222–229.
   PubMed Web of Science ®Google Scholar
• Dastgerdi HH, Radahmadi M, Reisi P. Comparative study of the protective effects of crocin and exercise on long-term potentiation of CA1 in rats under chronic unpredictable stress. Life Sci. 2020;256:1–10. 118018.
   Web of Science ®Google Scholar
• Hosseinzadeh H, Sadeghnia HR, Ghaeni FA, Motamedshariaty VS, Mohajeri SA, et al. Effects of saffron (Crocus sativus L.) and its active constituent, crocin, on recognition and spatial memory after chronic cerebral hypoperfusion in rats. Phytother Res. 2012;26:381–386.
   PubMed Web of Science ®Google Scholar
• Hadipour M, Kaka G, Bahrami F, Meftahi GH, Pirzad Jahromi G, Mohammadi A, Sahraei H, et al. Crocin improved amyloid beta induced long-term potentiation and memory deficits in the hippocampal CA1 neurons in freely moving rats. Synapse. 2018;72: e22026.
   PubMed Web of Science ®Google Scholar
• Samad N, Saleem A, Yasmin F, Shehzad MA, et al. Quercetin protects against stress-induced anxiety- and depression-like behavior and improves memory in male mice. Physiol Res. 2018;67:795–808.
   PubMed Web of Science ®Google Scholar
• Roozendaal B, Barsegyan A, Lee S. Adrenal stress hormones, amygdala activation, and memory for emotionally arousing experiences. Prog Brain Res. 2007;167:79–97.
   Web of Science ®Google Scholar
• Xiao Q, Xiong Z, Yu C, Zhou J, Shen Q, Wang L, et al. Antidepressant activity of crocin-I is associated with amelioration of neuroinflammation and attenuates oxidative damage induced by corticosterone in mice. Physiol Behav. 2019;212: 112699.
   Google Scholar
• Georgiadou G, Grivas V, Tarantilis PA, Pitsikas N, et al. Crocins, the active constituents of Crocus sativus L., counteracted ketamine-induced behavioural deficits in rats. Psychopharmacology (Berl). 2014;231:717–726.
   PubMed Web of Science ®Google Scholar
• Lechtenberg M, Schepmann D, Niehues M, Hellenbrand N, Wünsch B, Hensel A, et al. Quality and functionality of saffron: quality control, species assortment and affinity of extract and isolated saffron compounds to NMDA and sigma1 (sigma-1) receptors. Planta Med. 2008;74:764–772.
   PubMed Web of Science ®Google Scholar
• Ghasemi T, Abnous K, Vahdati F, et al. Antidepressant effect of Crocus sativus aqueous extract and its effect on CREB, BDNF, and VGF transcript and protein levels in Rat hippocampus. Drug Res (Stuttg). 2015;65:337–343.
   PubMed Web of Science ®Google Scholar