Alpha-Amylase Inhibitory and Antioxidant Activity of Red Galls Induced by Forda riccobonii in Pistacia atlantica Desf. Leaves: In vitro and In silico Studies
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Abstract
Pistacia atlantica has been widely used as a herbal remedy in the Mediterranean and the Middle East since antiquity. P. atlantica has been used as an antidiabetic drug plant in Arabic folk medicine. This study aims to determine the hypoglycemic and antioxidant activities of the gall part induced by Forda riccobonii in P. atlantica leaves from Algeria. Hypoglycemic activity was determined by measuring alpha-amylase inhibition activity using spectrophotometric analysis of extracts. Antioxidant activity was determined by DPPH, ABTS scavenging assay and FRAP reducing assays. A molecular docking study was carried out on compounds previously isolated from leaves using AutoDock vina software. The highest total phenolic content (655.49±18.36 mg GAE/g DM) and flavonoid content (381.30±15.47 mg QE/g DM) were detected in the butanol fraction. Based on the DPPH assays the ethyl acetate and butanol fractions had high antioxidant activities with EC50 2.46 and 9.94 µg/mL respectively. According to the ABTS assay, the best antioxidant activities were for the 35% MeOH-H2O (4.22 µg/mL) and ethyl acetate fractions (7.23 µg/mL). The α-amylase inhibitory activity was highest in the ethyl acetate fraction (IC50 64.53±2.50 µg/mL) followed by the positive control acarbose (78.98±6.23 µg/mL) and butanol
fraction, (151.85±3.01 µg/mL). The in silico study of compounds 5,6,7,4'-tetra-hydroxy-flavonol- 3-O-rutinoside and 3',5,7-tri-hydroxy-4'-methoxy-flavanone gave the best docking score (-8,3491 Kcal/mol and -8,1583 Kcal/mol, respectively). Finally, the in silico studies have confirmed significant α-amylase inhibitory activity with these molecules. As well as, the ADMET properties of these molecules appeared to be non-carcinogenic and non-hepatotoxic. Therefore, the gall's extract of P. atlantica could be used in the treatment of diabetes.
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Bailey CJ. New approaches to the pharmacotherapy of diabetes. In: Pickup JC, Williams G (Eds) Textbook of Diabetes. (3rd Ed). Oxford: Blackwell; 2003. 73.1–73.21 p.
Unuofin JO, Lebelo SL. Antioxidant effects and mechanisms of medicinal plants and their bioactive compounds for the prevention and treatment of type 2 diabetes: an updated review. Oxid Med Cell Longev. 2020; 2020: 1-36.
Bailey CJ, Krentz AJ. Oral antidiabetic agents. In: Holt RIG, Cockram CS, Flyvbjerg A, Goldstein BJ (Eds). Textbook of diabetes. (4th ed). Wiley-Blackwell; 2010. 452-477 p.
Amara M, Bouazza M, Errouane K, Kaid-Harche M, Nafil D, Pascalau R, Smuleac L, Al-Saghir MG. Systematic Position of Pistacia atlantica Desf. Subsp. atlantica in
North-West Algeria: Anatomy and Biometry of Leaves. Adv Res Life Sci. 2020; 4(1): 48-53.
Karimi A, Moradi M-T, Gafourian A. In vitro antiadenovirus activity and antioxidant potential of Pistacia atlantica Desf. leaves. Res J Pharmacog. 2020; 7(2): 53-60.
Sifi I, Yousfi M. Antimicrobial activity of essential oil from galls of Pistacia atlantica Desf. growing in Algeria. Phytotherapy. 2020; 18(6): 399-406.
Dousti M, Sari S, Saffari M, Kelidari H, Asare-Addo K, Nokhodchi A. Loading Pistacia atlantica essential oil in solid lipid nanoparticles and its effect on apoptosis of breast cancer cell line MDA-MB-231. Pharm Dev Technol. 2022; 27(1): 63-71.
Benmohamed M, Guenane H, Messaoudi M, Zahnit W, Egbuna C, Sharifi-Rad M, Chouh A, Seghir BB, Rebiai A, Boubekeur S, Azli T, Harrat M, Sawicka B, Atanassova M,
Yousfi M. Mineral profile, antioxidant, anti-inflammatory, antibacterial, anti-urease and anti-α-amylase activities of the unripe fruit extracts of Pistacia atlantica. Molecules. 2023; 28(1): 349.
Sifi I, Yousfi M, Benarous K, Dzoyem JP, Eloff JN. Essential oil from galls formed on leaves of Pistacia atlantica Desf.: New in vitro and in silico studies of anti-inflammatory activities. S Afr J Bot. 2022; 144: 464-470.
Pekacar S, Deliorman Orhan D. Investigation of antidiabetic effect of Pistacia atlantica leaves by activity-guided
fractionation and phytochemical content analysis by LCQTOF-MS. Front Pharmacol. 2022; 13: 568.
Hosseini S, Nili-Ahmadabadi A, Nachvak SM, Dastan D, Moradi S, Abdollahzad H, Mostafai R. Antihyperlipidemic and antioxidative properties of Pistacia atlantica subsp. kurdica in streptozotocin-induced diabetic mice. Diabetes
Metab Syndr Obes. 2020; 13: 1231-1236.
Benamar H, Marouf A, Bennaceur M. Phytochemical composition, antioxidant and acetylcholinesterase inhibitory
activities of aqueous extract and fractions of Pistacia atlantica subsp. atlantica from Algeria. J Herbs Spices Med Plants. 2018; 24(3): 229-244.
Sifi I, Dzoyem JP, Ouinten M, Yousfi M, McGaw LJ, Eloff JN. Antimycobacterial, antioxidant and cytotoxic activities
of essential oil of gall of Pistacia atlantica Desf. from Algeria. Afr J Tradit Complement Altern Med. 2015; 12(3): 150-155.
J. Al-Hadid K, Abu-Irmaileh B, A. Harb A, Sharab A, Alhadid A. Acacia cyanophylla, Eucalyptus camaldulensis, and Pistacia atlantica Ethanol extracts revealed cytotoxicity of breast cancer cell lines. Trop J Nat Prod Res. 2021; 5(10): 1808-1815.
Russo RA, Plant galls of the western United States. Princeton University Press; 2021. 400 p.
Harris MO, Pitzschke A. Plants make galls to accommodate foreigners: some are friends, most are foes. New Phytol.
; 225(5): 1852-1872.
Louzabi S, Belhadj S, Merbah KZA, Brague NB. New observation of Geoica mimeuri (Gaumont 1930) and description of Forda riccobonii (Stefani 1899) on Pistacia atlantica Desf. in Algeria. Faun Entomol. 2020; 73: 145-157.
Al-Aboudi A, Afifi FU. Plants used for the treatment of diabetes in Jordan: A review of scientific evidence. Pharm Biol. 2011; 49(3): 221-239.
Ondua M, Njoya EM, Abdalla MA, McGaw LJ. Antiinflammatory and antioxidant properties of leaf extracts of
eleven South African medicinal plants used traditionally to treat inflammation. J Ethnopharmacol. 2019; 234: 27-35.
Sánchez-Rangel JC, Benavides J, Heredia JB, CisnerosZevallos L, Jacobo-Velázquez DA. The Folin–Ciocalteu assay revisited: improvement of its specificity for total
phenolic content determination. Anal Methods. 2013; 5(21): 5990-5999.
Adebiyi OE, Olayemi FO, Ning-Hua T, Guang-Zhi Z. In vitro antioxidant activity, total phenolic and flavonoid contents of ethanol extract of stem and leaf of Grewia
carpinifolia. Beni-Suef Univ J basic Appl Sci. 2017; 6(1): 10-14.
Molyneux P. The use of the stable free radical diphenylpicrylhydrazyl (DPPH) for estimating antioxidant activity. Songklanakarin J. Sci. Technol. 2004; 26(2): 211-219.
Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, RiceEvans C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med. 1999; 26(9-10): 1231-1237.
Berker KI, Guclu K, Tor I, Apak R. Comparative evaluation of Fe(III) reducing power-based antioxidant capacity assays
in the presence of phenanthroline, batho-phenanthroline, tripyridyltriazine (FRAP), and ferricyanide reagents. Talanta. 2007; 72(3): 1157-1165.
Toul F, Moussouni S, Ghembaza N, Zitouni A, Djendar A, Atik-Bekkara F, Kokkalou E. Identification of phenolic
compounds in the buds of Algerian Pistacia atlantica Desf. Subsp. atlantica by antioxidant activity guided fractionation.
J Complement Integr Med. 2022; 19(2): 219-224.
Kim S, Thiessen PA, Bolton EE, Chen J, Fu G, Gindulyte A, Han L, He J, He S, Shoemaker BA. PubChem substance and
compound databases. Nucleic Acids Res. 2016; 44(D1): D1202-D1213.
Trott O, Olson AJ. AutoDock Vina: improving the speed and accuracy of Docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem. 2010; 31(2): 455-461.
Daina A, Michielin O, and Zoete V. SwissADME: a free web tool to evaluate pharmacokinetics, drug-likeness and
medicinal chemistry friendliness of small molecules. Sci Rep. 2017; 7: 1-13.
Banerjee P, Eckert AO, Schrey AK, Preissner R. ProTox-II: a webserver for the prediction of toxicity of chemicals.
Nucleic Acids Res. 2018; 46(W1): W257-W263.
Belyagoubi L, Belyagoubi-Benhammou N, Atik-Bekkara F, Coustard J. Effects of extraction solvents on phenolic content
and antioxidant properties of Pistacia atlantica Desf fruits from Algeria. Inter Food Res J. 2016; 23(3): 948-953.
Chaves JO, de Souza MC, da Silva LC, Lachos-Perez D, Torres-Mayanga PC, Machado APdF, Forster-Carneiro T,
Vázquez-Espinosa M, González-de-Peredo AV, Barbero GF, Rostagno MA. Extraction of flavonoids from natural sources using modern techniques. Front Chem. 2020; 8: 1-25.
Dirar AI, Alsaadi DHM, Wada M, Mohamed MA, Watanabe T, Devkota HP. Effects of extraction solvents on total
phenolic and flavonoid contents and biological activities of extracts from Sudanese medicinal plants. S Afr J Bot. 2019; 120: 261-267.
Toul F, Belyagoubi-Benhammou N, Zitouni A, AtikBekkara F. Antioxidant activity and phenolic profile of different organs of Pistacia atlantica Desf. subsp. atlantica from Algeria. Nat Prod Res. 2017; 31(6): 718-723.
Chelghoum M, Guenane H, Tahri D, Laggoun I, Marfoua FZ, Rahmani FZ, Khenifer F, Yousfi M. Influence of altitude,
precipitation, and temperature factors on the phytoconstituents, antioxidant, and α-amylase inhibitory activities of Pistacia atlantica. J Food Meas Charac. 2021; 15(5): 4411-4425.
Hatamnia AA, Rostamzad A, Hosseini M, Abbaspour N, Darvishzadeh R, Malekzadeh P, Aminzadeh BM. Antioxidant capacity and phenolic composition of leaves from 10 Bene (Pistacia atlantica subsp. kurdica) genotypes. Nat Prod Res. 2016; 30(5): 600-604.
Tsujita T. Persimmon-tannin, an alpha-amylase inhibitor, retards carbohydrate absorption in rats. J Nutr Sci Vitaminol.
(Tokyo). 2016; 62(3): 192-197.
Correa VG, Garcia-Manieri JAA, Silva AR, Backes E, Corrêa RCG, Barros L, Bracht A, Peralta RM. Exploring the α-amylase-inhibitory properties of tannin-rich extracts of Cytinus hypocistis on starch digestion. Food Res Int. 2023; 173(pt 1): 1-12.
Li K, Yao F, Du J, Deng X, Li C. Persimmon tannin decreased the glycemic response through decreasing the
digestibility of starch and inhibiting α-amylase, α-glucosidase, and intestinal glucose uptake. J Agric Food
Chem. 2018; 66(7): 1629-1637.
Kato CG, Gonçalves GdA, Peralta RA, Seixas FAV, de Sá-Nakanishi AB, Bracht L, Comar JF, Bracht A, Peralta RM. Inhibition of α-amylases by condensed and hydrolysable tannins: focus on kinetics and hypoglycemic actions. Enzyme Res. 2017; 2017: 1-13.
Elya B, Handayani R, Sauriasari R, Azizahwati, Hasyyati US, Permana IT, Permatasari YI. Antidiabetic activity and
phytochemical screening of extracts from Indonesian plants by inhibition of alpha-amylase, alpha glucosidase and dipeptidyl peptidase IV. Pak J Biol Sci. 2015; 18(6): 273-278.
Chu W-T, Wang J. Energy landscape topography reveals the underlying link between binding specificity and activity of
enzymes. Sci Rep. 2016; 6: 1-9.
Yadav VK, Mishra A. In vitro & in silico study of hypoglycemic potential of Pterocarpus marsupium heartwood extract. Nat Prod Res. 2019; 33(22): 3298-3302.
Lipinski CA. Lead- and drug-like compounds: the rule-offive revolution. Drug Discov Today Technol. 2004; 1(4):
-341.