Abstract
The Amygdalus spinosissima (Rosaceae) plant has been used in the Iranian folk medicine as a remedy for the burn wound. Hence, in this study, we aimed to determine the possible medicinal potential of the plant focusing on the root part. The bioactive phenolic and flavonoid compounds present in the root extract of the Amygdalus spinosissima plant as well as its antioxidant and anti-inflammatory properties were determined. Moreover, the effects of root extract on learning and memory in mice were evaluated. The results revealed that the root methanolic extract contained phenolic and flavonoid compounds including apigenin, quercetin, rutin, kaempferol, gallic acid, syringic acid, ferulic acid, and ellagic acid. The extract possessed antioxidant, acetylcholinesterase (AChE), and butyrylcholinesterase (BChE) inhibitory activities in vitro. These biological activities were attributed to the presence of phenolics and flavonoids. The A. spinosissima root extract improved learning and memory function in scopolamine-induced memory dysfunction in mice as determined using the Morris water maze task. The extract modulated the AChE, BChE, and inflammatory genes and enhanced the expression of the antioxidant enzymes in the brain. Consequently, A. spinosissima root extract could be considered as a promising source of potent bioactive compounds in the retarding the development of neurodegenerative diseases such as Alzheimer's disease.
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References
Ahmed U et al (2017) Physiochemical characteristics and fatty acid composition of Amygdalus Spinosissima seed oil from Balochistan. Indo Am J Pharm Sci 4:2755–2761
Akinyemi AJ, Oboh G, Fadaka AO, Olatunji BP, Akomolafe SJN (2017) Curcumin administration suppress acetylcholinesterase gene expression in cadmium treated rats. Neurotoxicology 62:75–79
Audas TE, Hardy-Smith PW, Penney J, Taylor T, Lu R (2016) Characterization of nuclear foci-targeting of Luman/CREB3 recruitment factor (LRF/CREBRF) and its potential role in inhibition of herpes simplex virus-1 replication. Eur J Cell Biol 95:611–622
Berg J, Tymoczko J, Stryer L (2002) Enzymes can be inhibited by specific molecules. Biochemistry, 5th edn. W H Freeman, New York
Bhattacharya S (2015) Reactive oxygen species and cellular defense system. In: Rani V, Yadav UCS (eds) Free radicals in human health and disease. Springer, India. https://doi.org/10.1007/978-81-322-2035-0_2
Budzynska B, Boguszewska-Czubara A, Kruk-Slomka M, Skalicka-Wozniak K, Michalak A, Musik I, Biala G (2015) Effects of imperatorin on scopolamine-induced cognitive impairment and oxidative stress in mice. Psychopharmacology 232:931–942
Bursal E, Aras A, Kılıç Ö, Taslimi P, Gören AC, Gülçin İ (2019) Phytochemical content, antioxidant activity, and enzyme inhibition effect of Salvia eriophora Boiss. & Kotschy against acetylcholinesterase, α‐amylase, butyrylcholinesterase, and α‐glycosidase enzymes. J Food Biochem 43:e12776
Cass SP (2017) Alzheimer’s disease and exercise: a literature review. Curr Sports Med Rep 16:19–22
Chen J, Long Y, Han M, Wang T, Chen Q, Wang R (2008) Water-soluble derivative of propolis mitigates scopolamine-induced learning and memory impairment in mice. Pharmacol Biochem Behav 90:441–446
Crozier A, Jaganath IB, Clifford MN (2006) Phenols, polyphenols and tannins: An overview. In: Plant Secondary Metabolites. Blackwell Publishing Ltd, pp 1–24. https://doi.org/10.1002/9780470988558.ch1
Crozier A, Jensen E, Lean M, McDonald M (1997) Quantitative analysis of flavonoids by reversed-phase high-performance liquid chromatography. J Chromatogr A 761:315–321
Freyssin A, Page G, Fauconneau B, Bilan AR (2018) Natural polyphenols effects on protein aggregates in Alzheimer’s and Parkinson’s prion-like diseases. Neural Regen Res 13:955
Grzesik M, Bartosz G, Dziedzic A, Narog D, Namiesnik J, Sadowska-Bartosz I (2018) Antioxidant properties of ferrous flavanol mixtures. Food Chem 268:567–576
Heim KE, Tagliaferro AR, Bobilya DJ (2002) Flavonoid antioxidants: chemistry, metabolism and structure-activity relationships. J Nutr Biochem 13:572–584
Hosseinzadeh H, Sadeghnia HR, Ghaeni FA, Motamedshariaty VS, Mohajeri SA (2012) Effects of saffron (Crocus sativus L.) and its active constituent, crocin, on recognition and spatial memory after chronic cerebral hypoperfusion in rats. Phytother Res 26:381–386
Ishola IO, Tota S, Adeyemi OO, Agbaje EO, Narender T, Shukla R (2013) Protective effect of Cnestis ferruginea and its active constituent on scopolamine-induced memory impairment in mice: a behavioral and biochemical study. Pharm Biol 51:825–835
Iskusnykh IY, Popova TN, Agarkov AA, de Carvalho P, Miguel Â, Rjevskiy SG (2013) Expression of glutathione peroxidase and glutathione reductase and level of free radical processes under toxic hepatitis in rats. J Toxicol. https://doi.org/10.1155/2013/870628
Ismail HI, Chan KW, Mariod AA, Ismail M (2010) Phenolic content and antioxidant activity of cantaloupe (Cucumis melo) methanolic extracts. Food Chem 119:643–647
Jung IH et al (2014) Ameliorating effect of spinosin, a C-glycoside flavonoid, on scopolamine-induced memory impairment in mice. Pharmacol Biochem Behav 120:88–94
Karimi E, Jaafar HZ, Ghasemzadeh A (2016) Chemical composition, antioxidant and anticancer potential of Labisia pumila variety alata under CO2 enrichment. NJAS-Wagening J Life Sci 78:85–91
Karimi E, Mehrabanjoubani P, Homayouni-Tabrizi M, Abdolzadeh A, Soltani M (2018) Phytochemical evaluation, antioxidant properties and antibacterial activity of Iranian medicinal herb Galanthus transcaucasicus Fomin. J Food Meas Charact 12:433–440
Kathirvel E, Chen P, Morgan K, French SW, Morgan TR (2010) Oxidative stress and regulation of anti-oxidant enzymes in cytochrome P4502E1 transgenic mouse model of non-alcoholic fatty liver. J Gastroenterol Hepatol 25:1136–1143
Lee J-S et al (2015) Hippocampal memory enhancing activity of pine needle extract against Scopolamine-induced amnesia in a mouse model. Sci Rep 5:9651
Lee JC et al (2018) Vanillin improves scopolamine-induced memory impairment through restoration of ID1 expression in the mouse hippocampus. Mol Med Rep 17:4399–4405
Leong HY, Show PL, Lim MH, Ooi CW, Ling TC (2018) Natural red pigments from plants and their health benefits: a review. Food Rev Int 34:463–482
Lim DW, Son HJ, Um MY, Kim I-H, Han D, Cho S, Lee C-H (2016) Enhanced cognitive effects of demethoxycurcumin, a natural derivative of curcumin on scopolamine-induced memory impairment in mice. Molecules 21:1022
Lorenzo JM, Munekata PE, Gomez B, Barba FJ, Mora L, Perez-Santaescolastica C, Toldra F (2018) Bioactive peptides as natural antioxidants in food products–a review. Trends Food Sci Technol 79:136–147
Lu C et al (2018) Genistein ameliorates scopolamine-induced amnesia in mice through the regulation of the cholinergic neurotransmission, antioxidant system and the ERK/CREB/BDNF signaling. Front Pharmacol 9:1153
Medina-Remón A, Kirwan R, Lamuela-Raventós RM, Estruch R (2018) Dietary patterns and the risk of obesity, type 2 diabetes mellitus, cardiovascular diseases, asthma, and neurodegenerative diseases. Crit Rev Food Sci Nutr 58:262–296
Orhan I, Kartal M, Tosun F, Şener B (2007) Screening of various phenolic acids and flavonoid derivatives for their anticholinesterase potential. Z Naturforsch C J Biosci 62:829–832
Oskoueian E, Abdullah N, Hendra R, Karimi E (2011) Bioactive compounds, antioxidant, xanthine oxidase inhibitory, tyrosinase inhibitory and anti-inflammatory activities of selected agro-industrial by-products. Int J Mol Sci 12:8610–8625
Oskoueian A, Haghighi RS, Ebrahimi M, Oskoueian E (2012) Bioactive compounds, antioxidant, tyrosinase inhibition, xanthine oxidase inhibition, anticholinesterase and anti inflammatory activities of Prunus mahaleb L. seed. J Med Plants Res 6:225–233
Oskoueian E, Karimi E, Noura R, Ebrahimi M, Shafaei N, Karimi E (2020) Nanoliposomes encapsulation of enriched phenolic fraction from pistachio hulls and its antioxidant, anti-inflammatory, and anti-melanogenic activities. J Microencapsul 37:1–13
Pisoschi AM, Pop A (2015) The role of antioxidants in the chemistry of oxidative stress: a review. Eur J Med Chem 97:55–74
Rabiei Z, Mokhtari S, Asgharzade S, Gholami M, Rahnama S, Rafieian-Kopaei M (2015) Inhibitory effect of Thymus vulgaris extract on memory impairment induced by scopolamine in rat. Asian Pac J Trop Biomed 5:845–851
Rendeiro C, Spencer JP, Vauzour D, Butler LT, Ellis JA, Williams CMJG, nutrition, (2009) The impact of flavonoids on spatial memory in rodents: from behaviour to underlying hippocampal mechanisms. Genes Nutr 4:251
Rice-Evans CA, Miller NJ, Paganga G (1996) Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic Biol Med 20:933–956
Rohn S, Rawel HM, Kroll J (2002) Inhibitory effects of plant phenols on the activity of selected enzymes. J Agric Food Chem 50:3566–3571
Saniewski M, Ueda J, Miyamoto K, Horbowicz M, Puchalski J (2006) Hormonal control of gummosis in Rosaceae. J Fruit Ornam Plant Res 14:137
Szwajgier D, Medicine E (2015) Anticholinesterase activity of selected phenolic acids and flavonoids-interaction testing in model solutions. Ann Agric Environ Med 22(4):690–694
Zaki HF, Abd-El-Fattah MA, Attia AS (2014) Naringenin protects against scopolamine-induced dementia in rats. Bull Facult Pharm, Cairo Univ 52:15–25
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Study design and experimental work were conducted by M. Sajjadi under the supervision of E. Oskoueian and E. Karimi. The in vitro and in vivo studies were carried out by M. Sajjadi and M. Ebrahimi. All authors reviewed and approved the final version of the manuscript.
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Sajjadi, M., Oskoueian, E., Karimi, E. et al. Amygdalus spinosissima root extract enhanced scopolamine-induced learning and memory impairment in mice. Metab Brain Dis 36, 1859–1869 (2021). https://doi.org/10.1007/s11011-021-00768-7
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DOI: https://doi.org/10.1007/s11011-021-00768-7