Combined effects of royal jelly and environmental enrichment against stress-induced cognitive and behavioral alterations in male rats: behavioral and molecular studies

References

• Lupien SJ, McEwen BS, Gunnar MR, Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci. 2009;10(6):434–45.
   PubMed Web of Science ®Google Scholar
• Horovitz O, Tsoory M, Hall J, Jacobson-Pick S, Richter-Levin G. Post-weaning to pre-pubertal (‘juvenile’) stress: a model of induced predisposition to stress-related disorders. Neuroendocrinology. 2012;95(1):56–64.
   PubMed Web of Science ®Google Scholar
• McEwen BS. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev. 2007;87(3):873–904.
   PubMed Web of Science ®Google Scholar
• Klenerová V, Jurčovičová J, Kaminský O, Šıda P, Krejčı́ I, Hliňák Z, et al. Combined restraint and cold stress in rats: effects on memory processing in passive avoidance task and on plasma levels of ACTH and corticosterone. Behav Brain Res. 2003;142(1-2):143–9.
   PubMed Web of Science ®Google Scholar
• Djordjevic J, Cvijic G, Davidovic V. Different activation of ACTH and corticosterone release in response to various stressors in rats. Physiol Res. 2003;52(1):67–72.
   PubMed Web of Science ®Google Scholar
• Broca P. Comparative anatomy of the cerebral convolutions: The great limbic lobe and the limbic fissure in the mammalian series. J Comp Neurol. 2015;523(17):2501–54.
   PubMed Web of Science ®Google Scholar
• Deveci A, Aydemir O, Taskin O, Taneli F, Esen-Danaci A. Serum BDNF levels in suicide attempters related to psychosocial stressors: a comparative study with depression. Neuropsychobiology. 2007;56(2-3):93–7.
   PubMed Web of Science ®Google Scholar
• Sperry M, Kandel B, Wehrli S, Bass K, Das S, Dhillon P, et al. Mapping of pain circuitry in early post-natal development using manganese-enhanced MRI in rats. Neuroscience. 2017;352:180–9.
   PubMed Web of Science ®Google Scholar
• Murínová J, Hlaváčová N, Chmelová M, Riečanský I. The evidence for altered BDNF expression in the brain of rats reared or housed in social isolation: a systematic review. Front Behav Neurosci. 2017;11:101.
   PubMed Web of Science ®Google Scholar
• Jawahar MC, Murgatroyd C, Harrison EL, Baune BT. Epigenetic alterations following early postnatal stress: a review on novel aetiological mechanisms of common psychiatric disorders. Clin Epigenetics. 2015;7(1):1–13.
   PubMedGoogle Scholar
• Nithianantharajah J, Hannan AJ. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci. 2006;7(9):697–709.
   PubMed Web of Science ®Google Scholar
• Angelucci F, De Bartolo P, Gelfo F, Foti F, Cutuli D, Bossù P, et al. Increased concentrations of nerve growth factor and brain-derived neurotrophic factor in the rat cerebellum after exposure to environmental enrichment. The Cerebellum. 2009;8(4):499–506.
   PubMed Web of Science ®Google Scholar
• Ramadan MF, Al-Ghamdi A. Bioactive compounds and health-promoting properties of royal jelly: A review. J Funct Foods. 2012;4(1):39–52.
   Web of Science ®Google Scholar
• You M-M, Chen Y-F, Pan Y-M, Liu Y-C, Tu J, Wang K, et al. Royal jelly attenuates LPS-induced inflammation in BV-2 microglial cells through modulating NF-κB and p38/JNK signaling pathways. Mediat Inflamm. 2018;2018.
   PubMed Web of Science ®Google Scholar
• Hattori N, Ohta S, Sakamoto T, Mishima S, Furukawa S. Royal jelly facilitates restoration of the cognitive ability in trimethyltin-intoxicated mice. Evidence-Based Complementary Altern Med. 2011;2011.
   PubMed Web of Science ®Google Scholar
• Hashimoto M, Kanda M, Ikeno K, Hayashi Y, Nakamura T, Ogawa Y, et al. Oral administration of royal jelly facilitates mRNA expression of glial cell line-derived neurotrophic factor and neurofilament H in the hippocampus of the adult mouse brain. Biosci, Biotechnol, Biochem. 2005;69(4):800–5.
   PubMed Web of Science ®Google Scholar
• Hattori N, Nomoto H, Fukumitsu H, Mishima S, Furukawa S. Royal jelly-induced neurite outgrowth from rat pheochromocytoma PC12 cells requires integrin signal independent of activation of extracellular signalregulated kinases. Biomed Res. 2007;28(3):139–46.
   PubMed Web of Science ®Google Scholar
• Hattori N, Nomoto H, Fukumitsu H, Mishima S, Furukawa S. Royal jelly and its unique fatty acid, 10-hydroxy-trans-2-decenoic acid, promote neurogenesis by neural stem/progenitor cells in vitro. Biomed Res. 2007;28(5):261–6.
   PubMed Web of Science ®Google Scholar
• Hattori N, Nomoto H, Fukumitsu H, Mishima S, Furukawa S. AMP N1-oxide, a unique compound of royal jelly, induces neurite outgrowth from pc12 vells via signaling by protein kinase A independent of that by mitogen-activated protein kinase. Evidence-Based Complementary Altern Med. 2010;7(1):63–8.
   PubMed Web of Science ®Google Scholar
• Teixeira RR, de Souza AV, Peixoto LG, Machado HL, Caixeta DC, Vilela DD, et al. Royal jelly decreases corticosterone levels and improves the brain antioxidant system in restraint and cold stressed rats. Neurosci Lett. 2017;655:179–85.
   PubMed Web of Science ®Google Scholar
• Pan Y, Xu J, Jin P, Yang Q, Zhu K, You M, et al. Royal jelly ameliorates behavioral deficits, cholinergic system deficiency, and autonomic nervous dysfunction in ovariectomized cholesterol-fed rabbits. Molecules. 2019;24(6):1149.
   Web of Science ®Google Scholar
• Mohamed AA-R, Galal AA, Elewa YH. Comparative protective effects of royal jelly and cod liver oil against neurotoxic impact of tartrazine on male rat pups brain. Acta Histochem. 2015;117(7):649–58.
   PubMed Web of Science ®Google Scholar
• Ito S, Nitta Y, Fukumitsu H, Soumiya H, Ikeno K, Nakamura T, et al. Antidepressant-like activity of 10-hydroxy-trans-2-decenoic acid, a unique unsaturated fatty acid of royal jelly, in stress-inducible depression-like mouse model. Evidence-Based Complementary Altern Med. 2012;2012.
   Web of Science ®Google Scholar
• Moradi-Kor N, Dadkhah M, Ghanbari A, Rashidipour H, Bandegi AR, Barati M, et al. Protective effects of spirulina platensis, voluntary exercise and environmental interventions against adolescent stress-induced anxiety and depressive-like symptoms, oxidative stress and alterations of BDNF and 5HT-3 receptors of the prefrontal cortex in female rats. Neuropsychiatr Dis Treat. 2020;Volume 16:1777.
   Web of Science ®Google Scholar
• Moradi-Kor N, Ghanbari A, Rashidipour H, Yousefi B, Bandegi AR, Rashidy-Pour A. Beneficial effects of Spirulina platensis, voluntary exercise and environmental enrichment against adolescent stress induced deficits in cognitive functions, hippocampal BDNF and morphological remolding in adult female rats. Horm Behav. 2019;112:20–31.
   PubMed Web of Science ®Google Scholar
• Sakhaie N, Sadegzadeh F, Mohammadnia A, Dadkhah M, Saadati H. Sex-dependent effects of postweaning exposure to an enriched environment on novel objective recognition memory and anxiety-like behaviors: The role of hippocampal BDNF level. Int J Dev Neurosci. 2020;80(5):396–408.
   Web of Science ®Google Scholar
• Sadegzadeh F, Sakhaie N, Isazadehfar K, Saadati H. Effects of exposure to enriched environment during adolescence on passive avoidance memory, nociception, and prefrontal BDNF level in adult male and female rats. Neurosci Lett. 2020;732:135133.
   PubMed Web of Science ®Google Scholar
• Hajali V, Sheibani V, Ghazvini H, Ghadiri T, Valizadeh T, Saadati H, et al. Effect of castration on the susceptibility of male rats to the sleep deprivation-induced impairment of behavioral and synaptic plasticity. Neurobiol Learn Mem. 2015;123:140–8.
   PubMed Web of Science ®Google Scholar
• Shafia S, Vafaei AA, Samaei SA, Bandegi AR, Rafiei A, Valadan R, et al. Effects of moderate treadmill exercise and fluoxetine on behavioural and cognitive deficits, hypothalamic-pituitary-adrenal axis dysfunction and alternations in hippocampal BDNF and mRNA expression of apoptosis–related proteins in a rat model of post-traumatic stress disorder. Neurobiol Learn Mem. 2017;139:165–78.
   PubMed Web of Science ®Google Scholar
• De Kloet ER, Joëls M, Holsboer F. Stress and the brain: from adaptation to disease. Nat Rev Neurosci. 2005;6(6):463–75.
   PubMed Web of Science ®Google Scholar
• Miller WL. StAR search—what we know about how the steroidogenic acute regulatory protein mediates mitochondrial cholesterol import. Mol Endocrinol. 2007;21(3):589–601.
   PubMedGoogle Scholar
• Paula-Freire LI, Mendes FR, Molska GR, Duarte-Almeida JM, Carlini EA. Comparison of the chemical composition and biological effects of the roots, branches and leaves of Heteropterys tomentosa A. Juss. J Ethnopharmacol. 2013;145(2):647–52.
   PubMed Web of Science ®Google Scholar
• Patki G, Allam F, Bohat R, Jafri F, Saleem M, Salim S. Role of oxidative stress in anxiety-like behavior and learning and memory impairment in a rat model of social stress. Wiley Online Library; New York, 2013.
   Google Scholar
• Lercker G, Capella P, Conte L, Ruini F, Giordani G. Components of royal jelly II. The lipid fraction, hydrocarbons and sterols. J Apic Res. 1982;21(3):178–84.
   Web of Science ®Google Scholar
• Jones D, Marante D, Williams B, Edwards C. Adrenal synthesis of corticosterone in response to ACTH in rats is influenced by leukotriene A4 and by lipoxygenase intermediates. J Endocrinol. 1987;112(2):253–8.
   PubMed Web of Science ®Google Scholar
• Kamakura M, Moriyama T, Sakaki T. Changes in hepatic gene expression associated with the hypocholesterolaemic activity of royal jelly. J Pharm Pharmacol. 2010;58(12):1683–9.
   Google Scholar
• Kashima Y, Kanematsu S, Asai S, Kusada M, Watanabe S, Kawashima T, et al. Identification of a novel hypocholesterolemic protein, major royal jelly protein 1, derived from royal jelly. PloS one. 2014;9(8):e105073.
   PubMed Web of Science ®Google Scholar
• Iegaki N, Narita Y, Hattori N, Hirata Y, Ichihara K. Royal jelly reduces depression-like behavior through possible effects on adrenal steroidogenesis in a murine model of unpredictable chronic mild stress. Biosci, Biotechnol, Biochem. 2020;84(3):606–12.
   PubMed Web of Science ®Google Scholar
• Pyrzanowska J, Piechal A, Blecharz-Klin K, Joniec-Maciejak I, Graikou K, Chinou J, et al. Administration of Greek Royal jelly produces fast response in neurotransmission of aged Wistar male rats. Journal of Pre-Clinical and Clinical Research. 2015;9(2).
   Google Scholar
• Moreira PS, Almeida PR, Leite-Almeida H, Sousa N, Costa P. Impact of chronic stress protocols in learning and memory in rodents: systematic review and meta-analysis. PLoS One. 2016;11(9):e0163245.
   PubMed Web of Science ®Google Scholar
• Chao MV, Rajagopal R, Lee FS. Neurotrophin signalling in health and disease. Clin Sci. 2006;110(2):167–73.
   PubMed Web of Science ®Google Scholar
• Novkovic T, Mittmann T, Manahan-Vaughan D. BDNF contributes to the facilitation of hippocampal synaptic plasticity and learning enabled by environmental enrichment. Hippocampus. 2015;25(1):1–15.
   PubMed Web of Science ®Google Scholar
• Sadegzadeh F, Sakhaie N, Dehghany R, Adak O, Saadati H. Effects of adolescent administration of fluoxetine on novel object recognition memory, anxiety-like behaviors, and hippocampal brain-derived neurotrophic factor level. Life Sci. 2020;260:118338.
   PubMed Web of Science ®Google Scholar
• Lee J, Seroogy KB, Mattson MP. Dietary restriction enhances neurotrophin expression and neurogenesis in the hippocampus of adult mice. J Neurochem. 2002;80(3):539–47.
   PubMed Web of Science ®Google Scholar
• Wolf SA, Kronenberg G, Lehmann K, Blankenship A, Overall R, Staufenbiel M, et al. Cognitive and physical activity differently modulate disease progression in the amyloid precursor protein (APP)-23 model of Alzheimer’s disease. Biol Psychiatry. 2006;60(12):1314–23.
   PubMed Web of Science ®Google Scholar
• Pavel CI, Mărghitaş LA, Bobiş O, Dezmirean DS, Şapcaliu A, Radoi I, et al. Biological activities of royal jelly-review. Scientific Papers Animal Sci Biotechnol. 2011;44(2):108–18.
   Google Scholar
• Greenwood BN, Strong PV, Foley TE, Fleshner M. A behavioral analysis of the impact of voluntary physical activity on hippocampus-dependent contextual conditioning. Hippocampus. 2009;19(10):988–1001.
   PubMed Web of Science ®Google Scholar
• Ting C-Y, Fan C-H, Liu H-L, Huang C-Y, Hsieh H-Y, Yen T-C, et al. Concurrent blood–brain barrier opening and local drug delivery using drug-carrying microbubbles and focused ultrasound for brain glioma treatment. Biomaterials. 2012;33(2):704–12.
   PubMed Web of Science ®Google Scholar