Identification of bioactive compounds from Fraxinus angustifolia extracts with antiNADH oxidase activity of bovine milk xanthine oxidoreductase

Identification of bioactive compounds from Fraxinus angustifolia extracts with antiNADH oxidase activity of bovine milk xanthine oxidoreductase

Fraxinus angustifolia leaves and bark are used in traditional medicine against various inflammatory-related pathologiesincumbent to reactive oxygen species (ROS) generation by the NADH oxidase activity of enzymes such as xanthine oxidoreductase(XOR). This study was designed to investigate the in vitro and in vivo inhibitory activities of this enzyme by Fraxinus angustifoliaextracts. The leaf organic phase of ethyl acetate (LFA) and its bark aqueous counterpart (BFA) showed the strongest anti-NADH oxidaseactivity in vitro (IC50 = 38.51 and 42.04 µg mL-1, respectively). They consequently suppressed superoxide generation both enzymatically(53% and 19%, respectively) and nonenzymatically (34% and 19%, respectively). These results were corroborated in vivo, with high antiNADH oxidase potential of the leaves and bark extracts (75.32% and 51.32%, respectively) concomitant with moderate hypouricemicactivities (36.84% and 38.59%, respectively). Bio-guided fractionation led to the identification, by LC-DAD-MS/MS, of esculin andcalcelarioside in bark and kaempferol glucoside in leaves as the main compounds responsible for the anti-NADH oxidase activity ofXOR. These results plead in favor of the use of F. angustifolia as a source of potentially interesting therapeutic substances.

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  • Abu-Reidah IM, ALI- Shtayeh MS, Jamous RM, Roman DA (2015). HPLC-DAD-ESI-MS/MS screening of bioactive components from Rhus coriaria L (Sumac) fruits. Food Chem 166: 179-191.
  • Atmani D, Baghiani A, Harrison R, Benboubetra M (2005). NADH oxidation and superoxide production by milk xanthine oxidoreductase. Int Dairy J 15: 1113-1121.
  • Atmani D, Chaher N, Berboucha M, Ayouni K, Lounis H, Boudaoud H, Debbache N, Atmani D (2009). Antioxidant capacity and phenol content of selected Algerian medicinal plants. Food Chem 112: 303-309.
  • Ayouni K, Berboucha-Rahmani M, Kim HK, Atmani D, Verpoorte R, Choi YH (2016). Metabolomic tool to identify antioxidant compounds of Fraxinus angustifolia leaf and stem bark extracts. Ind Crops Prod 88: 65-77.
  • Beloued A (1998). Plantes Médicinales d’Algérie. Algiers, Algeria: Office des Publications Universitaires (in French). Berboucha M, Ayouni K, Atmani D, Atmani D, Benboubetra M (2010). Kinetic study on the inhibition of xanthine oxidase by extracts from two selected Algerian plants traditionally used for the treatment of inflammatory diseases. J Med Food 1: 9-13.
  • Bindoli A, Valente M, Cavallini L (1985). Inhibitory action of quercetin on xanthine oxidase and xanthine dehydrogenase activity. Pharmacol Res Comm 17: 831-839.
  • Bradford MM (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
  • Cantu-Medellin N, KelleyE E (2013). Xanthine oxidoreductasecatalyzed reduction of nitrite to nitric oxide: insights regarding where, when and how. Nitric Oxide 34: 19-26.
  • Cao G, Sofic E, Prior RL (1997). Antioxidant and prooxidant behaviour of flavonoids: structure-activity relationships. Free Radic Biol Med 22: 749-760.
  • Chang WS, Chiang HC (1995). Structure-activity relationship of coumarins in xanthine oxidase inhibition. Anticancer Res 15: 1969-1974.
  • Cos P, Ying L, Calomme M, Hu JP, Cimanga K, Poel BV, Pieters L, Vlietinck AJ,Berghe DV (1998). Structure-activity relationship and classification of flavonoids as inhibitors of xanthine oxidase and superoxide scavengers. J Nat Prod 61: 71-76.
  • Dixon M (1972). The graphical determination of Km and Ki. Biochem J 129: 133-140.
  • Djerroumi A, Nacef M (2004). 100 Plantes médicinales d’Algérie. Palais du livre, pp 45-110.
  • Doroshow JH (1983). Anthracycline antibiotic-stimulated superoxide, hydrogen peroxide, and hydroxyl radical production by NADH dehydrogenase. Cancer Research 43: 4543-4551.
  • Enroth C, Eger BT, Okamoto K, Nishino T, Nishino T, Pai EP (2000). Crystal structures of bovine milk xanthine dehydrogenase and xanthine oxidase: structure-based mechanism of conversion. Proc Natl Acad Sci USA 97: 10723-10728.
  • Eyles A, William J, Riedl K, Cipollini D, Schwartz S, Chan K, Herms DA, Bonello P (2007). Comparative phloem chemistry of Manchurian (Fraxinus mandshurica) and two North American ash species (Fraxinus americana and Fraxinus pennsylvanica). J Chem Ecol 33: 1430-1448.
  • Frison-Norrie S, Sporns P (2002). Identification and quantification of flavonol glycosides in almond seed coats using MALDI-TOF MS. J Agric Food Chem 50: 2782-2787.
  • Granger DN, Stokes KY, Shigematsu T, Cerwinka WH, Tailer A, Krieglstein CF (2001). Splanchnic ischemia-reperfusion injury: mechanistic insights provided by mutant mice. Acta Physiol Scand 173: 83-91.
  • Hagerman AE, Bulter LG (1978). Protein precipitation method for the quantitative determination of tannins. J Agric Food Chem 26: 809-812.
  • Hamilton C, Brosnan M, McIntyre M, Graham D, Dominiczak A (2001). Superoxide excess in hypertension and aging, a common cause of endothelial dysfunction. J Hypertens 37: 529-534.
  • Haskard DO, Landis RC (2002). Interactions between leukocytes and endothelial cells in gout: lessons from a self-limiting inflammatory response. Arthritis Res 4: 91-94.
  • Hattori Y (1989). Localization of xanthine dehydrogenase in chicken liver. Acta Histochem Cytochem 22: 617-6924.
  • Iossifova T, Kostova I, Evstatieva LN (1997). Secoiridoids and hydroxycoumarins in Bulgarian Fraxinus species. Biochem Syst Ecol 25: 271-274.
  • Jenson SR, Franzyk H, Wallander E (2002). Chemotaxonomy of the oleaceae: iridoids as taxonomic markers. Phytochem 60: 213- 231.
  • Kong LD, Zhou J, Wen Y, Li J, Cheng CHK (2002). Aesculin possesses potent hypouricemic action in rodents but is devoid of xanthine oxidase/dehydrogenase inhibitory activity. Planta Med 68: 175-178.
  • Kostova I, Iossifova T (2007). Ch emical components of Fraxinus species. Fitoterapia 78: 85-106.
  • Li JM, Zhang X, Wang X, Xie YC, Kong LD (2011). Protective effects of cortex fraxini coumarines against oxonate-induced hyperuricemia and renal dysfunction in mice. Eur J Pharmacol 666: 196-204.
  • Lin KW, Chen YT, Yang SC, Wei BL, Hung CF, Lin CN (2013). Xanthine oxidase inhibitory lanostanoids from ganodermatsugae. Fitoterapia 89: 231-238.
  • LiuF, Ooi VE, Chang ST (1997). Free radical scavenging activities of mushroom polysaccharide extracts. Life Sci J 60: 763-771.
  • Lowman MD, Box J (1983). Variation in leaf toughness and phenolic content among five species of Australian rain forest trees. Austr J Ecol 8: 17-25.
  • Maia L, Duarte RO, Ponces-Freire A, Moura JJ, Mira L (2007). NADH oxidase activity of rat and human liver xanthine oxidoreductase: potential role in superoxide production. J Biol Inorg Chem 12: 777-787.
  • Maksimović Z, Malencie N, Kovacevie N (2005). Polyphenol contents and antioxidant activity of Maydis stigma extracts. Bioresour Technol 96: 873-877.
  • Medjahed Z, Atmani-Kilani D, Fauconnier ML, Richard G, Atmani D (2016). Hepatoprotective and anti-diabetic activities of Fraxinus angustifolia Vahl extracts in animal models: characterization by HPLC analysis. Turk J Med Sci 46: 910-920.
  • Michel T, Khlif I, Kanakis P, Termentzi A, Allouche N, Halabalaki M, Skaltsounis AL (2015). UHPLC-DAD-FLD and UHPLCHRMS/MS based metabolic profiling and characterization of different Olea europaea organs of Koroneiki and Chetoui varieties. Phytochem Lett 11: 424-439.
  • Moulaoui K, Caddeo C, Manca ML, Castangia I, Valenti D, Escribano E, Atmani D, Fadda AM, Manconi M (2015). Identification and nanoentrapment of polyphenolic phytocomplex from Fraxinus angustifolia: in vitro and in vivo wound healing potential. Eur J Med Chem 89: 179-188.
  • Naczk M, Shahidi F (2004). Extraction and analysis of phenolics in food. J Chromatogr A. 1054: 95-111.
  • Nagao A, Seki M, Kobayashi H (1999). Inhibition of xanthine oxidase by flavonoids. Biosci Biotechnol Biochem 63: 1787-1790.
  • Niemetz R, Gross GG (2001). Gallotannin biosynthesis: β-glucogallin: hexagalloyl 3-O-galloyltransferase from Rhus typhina leaves. Phytochem 58: 6657-6661.
  • Perez JA, Hernandez JM, Trujillo JM, Lopez H (2005). Iridiods and secoiridoids from Oleaceae. J Nat Prod Chem 32: 303-363.
  • Romani A, Pinelli P, Galardi C, Mulinacci N, Tattini M (2002). Identification and quantification of galloyl derivatives, flavonoides glycosides, and andantho-cyanins in leaves of Pistacia lentiscus L. Phytochem Anal 13: 79-86.
  • Ruiz A, Bustamante L, Vergara C, Baer DV, Gutiérrez IH, Obando L, Mardones C (2015). Hydroxycinnamic acids and flavonols in native edible berries of South Patagonia. Food Chem 90: 167- 184.
  • Russo A, Cardile V, Lombardo L, VanellaL, Vanella A,Garbarino JA (2005). Antioxidant and antiproliferative action of methanolic extract of Geumquellyon sweet roots in human tumor cell lines. J Ethnopharmacol 100: 323-332.
  • Sanders SA, Eisenthal R, Harrison R (1997). NADH oxidase activity of human xanthine oxidoreductase-generation of superoxide anion. Eur J Biochem 245: 541-548.
  • Sanz M, Simón BF, Cadahía E, Esteruelas E, Muñoz AM, Hernández T, Estrellac I, Pinto E (2012). LC-DAD/ESI-MS/MS study of phenolic compounds in ash Fraxinus excelsior L and F americana L heartwood effect of toasting intensity at cooperage. J Mass Spectrom 47: 905-918.
  • Silva MP, Mira L, Lima JV (1996). Kinetic of the inhibition of xanthine dehydrogenase and the reversible and irreversible forms of xanthine oxidase by Silibinin and bendazac. Environ Toxicol Pharmacol 1: 279-284.
  • So A, Thorens B (2010). Uric transport and disease. J Clin Invest 6: 791-799.
  • Sun H, Liu M, Lin Z, Jiang H,Niu Y, Wang H, Chen S (2015). Comprehensive identification of 125 multifarious constituents in Shuang-huang–lian powder injection by HPLC-DAD-ESIIT-TOF-MS. Pharmaceut Biomed 86: 106-115.
  • Teplova VV, Kruglov AG, Kovalyov LI, Nikiforova AB, Fedotcheva NI, Lemasters JJ (2017). Glutamate contributes to alcohol hepatotoxicity by enhancing oxidative stress in mitochondria. J Bioenerg Biomembr 49: 253-264.
  • Touhami H, Ghazghazi H, Sellimi H, Khaldi A, Mahmoudi H (2017). Antioxidant activities and phenolic contents of bark and leaves extracts from Tunisian native tree: Fraxinus angustifolia vahl. subsp. angustifolia. J Agri Biotech 45: 2286-5314.
  • Veličković DT, Nikolova MT, Ivancheva SV, Stojanovi JB, Veličković VB (2007). Extraction of flavonoids from garden (Salvia officinalis L.) and glutinous (Salvia glutinosa L.) sage by ultrasonic and classical maceration. J Serb Chem Soc 72: 73-80.
  • Vorbach C, Scriven A, Capecchi MR (2002). The housekeeping gene xanthine oxidoreductase is necessary for milk fat droplet enveloping and secretion: Gene sharing in the lactating mammary gland. Genes Dev 16: 3223-3235.
  • Wang CP, Wang X, Zhang X, Shi YW, Liu L, Kong LD (2010). Morin improves urate excretion and kidney function through regulation of renal organic ion transporters hyperuricemic mice. J Pharm Pharmaceut Csi 13: 411-427.
  • Waud WR, Rajagopalan KV (1976). Purification and properties of the NAD+-dependent (type D) and O2 -dependant (type O) forms of rat liver xanthine dehydrogenase. Arch Biochem Biophys 172: 354-364.
  • Younis T, Khan MR, Moniba, Sajid M (2016). Protective effects of Fraxinus xanthoxyloides (Wall) leaves against CCl4 induced hepatic toxicity in rat. BMC Complement Altern Med 2016: 16-407.
  • Zhu JX, Wang Y, Kong LD, Yang C, Zhang X (2004). Effects of Biota orientalis extract and its flavonoid constituents, quercetin and rutin on serum uric acid levels in oxonate-induced mice and xanthine dehydrogenase and xanthine oxidase activities in mouse liver. J Ethnopharmacol 93: 133-140.
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