New Sulphated Flavonoids from Tamarix africana and Biological Activities of Its Polar Extract

Abstract

The phytochemical investigation of Tamarix africana Poir. (Tamaricaceae) shoot polar extract afforded three new sulphated flavonoids, (2S,4R)-5,7,4′-trihydroxyflavan-4-ol 5,7-disulphate (1), (2S)-5,7,4′-trihydroxyflavan 7-O-sulphate (2), and (2S)-naringenin 4′-O-sulphate (3), together with ten known compounds. Their structures were determined by spectroscopic methods including 1D and 2D NMR analysis and HRMS. Biological activities of the polar extract of T. africana shoots related to its phenolic content were also investigated. A high total phenolic content (151.1 mg GAE/g) was found in the methanol shoot extract, which exhibits strong antioxidant activities using the oxygen radical absorbance capacity method and a skin cell-based assay. Moreover, the shoot extract showed significant anti-inflammatory activity, reducing nitric oxide release by 53.5 % at 160 µg/mL in lipopolysaccharide-stimulated RAW 264.7 macrophages. Finally, T. africana shoot extract inhibited the growth of A-549 lung carcinoma cells, with an IC₅₀ value of 34 µg/mL.

Key words

Tamarix africana - Tamaricaceae - sulphated flavonoids - antioxidant activity - cytotoxicity - anti-inflammatory activity

• References

• 1 Khabtane A, Rahmoune C. Effet du biotope sur la diversité floristique et le polymorphisme phénotypique des groupements à Tamarix africana Poir. Dans les zones arides de la région de Khenchela (Est Algérien). J Agr Environ Int Dev 2012; 106: 123-137
• 2 Ksouri R, Ksouri WM, Jallali I, Debez A, Magné C, Hiroko I, Abdelly C. Medicinal halophytes: potent source of health promoting biomolecules with medical, nutraceutical and food applications. Crit Rev Biotechnol 2012; 32: 289-326
• 3 Sharma V, Bhardwaj U, Sharma S, Sharma S. Medicinal plants: need for sustainable exploitation (with special reference to Himachal Pradesh). J Pharm Res 2012; 5: 4313-4317
• 4 Parmar VS, Bisht KS, Sharma SK, Jain R, Tanya P, Singh S, Simonsen O, Boll PM. Highly oxygenated bioactive flavones from Tamarix . Phytochemistry 1994; 36: 507-511
• 5 Ahmet A, Yurdanur A. A new analogue of fatty alcohol from Tamarix hampeana L. Nat Prod Res 2010; 24: 34-39
• 6 Sharma SK, Parmar VS. Novel constituents of Tamarix species. J Sci Ind Res 1998; 57: 873-890
• 7 Saïdana D, Mahjoub MA, Boussaada O, Chriaa J, Chéraif I, Daami M, Mighri Z, Helal AN. Chemical composition and antimicrobial activity of volatile compounds of Tamarix boveana (Tamaricaceae). Microbiol Res 2008; 163: 445-455
• 8 Nawwar MAM, Buddrus J, Bauer HL. Dimeric phenolic constituents from the roots of Tamarix nilotica . Phytochemistry 1982; 21: 1755-1758
• 9 Saleh NAM, El-Sissi HI. A rhamnetin glucuronide trisulphate from the leaves of Tamarix aphylla . Phytochemistry 1975; 14: 312-314
• 10 Younos C, Soulimani R, Seddiqi N, Baburi O, Dicho A. Étude ethnobotanique et historique des tamaris (Tamarix sp., Tamaricaceae) et leurs usages actuels en Afghanistan. Phytotherapie 2005; 3: 248-251
• 11 Falleh H, Oueslati S, Guyot S, Ben Dali A, Magné C, Abdelly C, Ksouri R. LC/ESI-MS/MS characterisation of procyanidins and propelargonidins responsible for the strong antioxidant activity of the edible halophyte Mesembryanthemum edule L. Food Chem 2011; 127: 1732-1738
• 12 Zhao Z, Ruan J, Jin J, Zou J, Zhou D, Fang W, Zeng F. Flavan-4-ol glycosydes from the rhizomes of Abacopteris penangiana . J Nat Prod 2006; 69: 265-268
• 13 Slade D, Ferreira D, Marais JPJ. Circular dichroism, a powerful tool for the assessment of absolute configuration of flavonoids. Phytochemistry 2005; 66: 2177-2215
• 14 Okamoto A, Ozawa T, Imagawa H, Arai Y. Flavans from the pith of sago palm. Agric Biol Chem 1986; 50: 1655-1656
• 15 Agrawal PK. Carbon-13 NMR of flavonoids. Amsterdam: Elsevier; 1989: 102
• 16 Ibrahim AR, Galal AM, Ahmed MS, Mossa GS. O-demethylation and sulfation of 7-methoxylated flavanones by Cunninghamella elegans . Chem Pharm Bull (Tokyo) 2003; 51: 203-206
• 17 Abdel-Mogib M, Basaif SA, Al-Garni SM. Antimicrobial activity and chemical constituents of leaf extracts of Tamarix aphylla . Alex J Pharm Sci 2001; 15: 121-123
• 18 Merfort I, Wendisch D. Flavonol glucuronide from the flowers of Arnica montana . Planta Med 1988; 54: 247-250
• 19 Pettit GR, Singh SB. Antineoplastic agents. Isolation, structure, and synthesis of combretastatin A-2, A-3, and B-2. Canad J Chem 1987; 65: 2390-2396
• 20 Tanaka M, Ikeya Y, Mitsuhashi H, Maruno M, Wakamatsu T. Total synthesis of the metabolites of schizandrin. Tetrahedron 1995; 51: 11703-11724
• 21 Nawwar MAM, Souleman AMA, Buddrus J, Linscheid M. Flavonoids of the flowers of Tamarix nilotica . Phytochemistry 1984; 23: 2347-2349
• 22 Dewanto V, Wu X, Adom KK, Liu RH. Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity. J Agric Food Chem 2002; 50: 3010-3014
• 23 Sun B, Richardo-da-Silvia M, Spranger I. Critical factors of vanillin assay for catechins and proanthocyanidins. J Agric Food Chem 1998; 46: 4267-4274
• 24 Karker M, Falleh H, Msaada K, Smaoui A, Abdelly C, Legault J, Ksouri R. Antioxidant, anti-inflammatory and anticancer activities of the medicinal halophyte Reaumuria vermiculata . EXCLI J 2016; 15: 297-307
• 25 Medini F, Bourgou S, Girard-Lalancette K, Snoussi M, Mkadmini K, Cot I, Abdelly C, Legault J, Ksouri R. Phytochemical analysis, antioxidant, anti-inflammatory, and anticancer activities of the halophyte Limonium densiflorum extracts on human cell lines and murine macrophages. S Afr J Bot 2015; 99: 158-164
• 26 Sanchez-Rodrıguez E, Moreno DA, Ferreres F, Rubio-Wilhelmi MM, Ruiz JM. Differential responses of five cherry tomato varieties to water stress: changes on phenolic metabolites and related enzymes. Phytochemistry 2011; 2: 723-729
• 27 Awika JM, Rooney LW, Wu X, Prior RL, Zevallos LC. Screening methods to measure antioxidant activity of sorghum (Sorghum bicolor) and Sorghum products . J Agric Food Chem 2003; 51: 6657-6662
• 28 Girard-Lalancette K, Pichette A, Legault J. Sensitive cell-based assay using DCFH oxidation for the determination of pro- and antioxidant properties of compounds and mixtures: analysis of fruit and vegetable juices. Food Chem 2009; 115: 720-726
• 29 Megdiche Ksouri W, Medini F, Mkadmini K, Legault J, Abdelly C, Ksouri R. LC-ESI-TOF-MS identification of bioactive secondary metabolites involved in the antioxidant, anti-inflammatory and anticancer activities of the edible halophyte Zygophyllum album Desf. Food Chem 2013; 139: 1073-1080
• 30 Tsai PJ, Tsai TH, Yu CH, Ho SC. Evaluation of NO suppressing activity of several Mediterranean culinary spices. Food Chem Toxicol 2007; 45: 440-447
• 31 Taira J, Nanbu H, Ueda K. Nitric oxide-scavenging compounds in Agrimonia pilosa Ledeb on LPS-induced RAW264.7 macrophages. Food Chem 2009; 115: 1221-1227
• 32 Oueslati S, Ksouri R, Falleh H, Pichette A, Abdelly C, Legault J. Phenolic content, antioxidant, anti-inflammatory and anticancer activities of the edible halophyte Suaeda fruticosa Forssk. Food Chem 2012; 132: 943-947
• 33 Nemeikaite-Ceniene A, Imbrasaite A, Sergediene E, Cenas N. Quantitative structure–activity relationships in prooxidant cytotoxicity of polyphenols: role of potential of phenoxyl radical/phenol redox couple. Arch Biochem Biophys 2005; 441: 182-190
• 34 Vuorela S, Kreander K, Karonen M, Nieminen R, Hämäläinen M, Galkin A, Laitinen L, Salminen JP, Moilanen E, Pihlaja K, Vuorela H, Vuorela P, Heinonen M. Preclinical evaluation of rapeseed, raspberry, and pine bark phenolics for health related effects. J Agric Food Chem 2005; 53: 5922-5931
• 35 Khalil A, Baltenweck-Guyot R, Ocampo-Torres R, Albrecht P. Retrodihydrochalcones in Sorghum species: key intermediates in the biosynthesis of 3-deoxyanthocyanidins?. Phytochem Lett 2012; 5: 174-176
• 36 Ou B, Hampsch-Woodill M, Prior RL. Development and validation of an improved oxygen radical absorbance capacity assay using fluorescein as the fluorescent probe. J Agric Food Chem 2001; 49: 4619-4626
• 37 Legault J, Dahl W, Debiton E, Pichette A, Madelmont JC. Antitumor activity of balsam fir oil: production of reactive oxygen species induced by alpha-humulene as possible mechanism of action. Planta Med 2003; 69: 402-407
• 38 Green SJ, Meltzer MS, Hibbs Jr. JB, Nacy CA. Activated macrophages destroy intracellular Leishmania major amastigotes by an L-arginine-dependent killing mechanism. J Immunol 1990; 144: 278-283
• 39 OʼBrien J, Wilson I, Orton T, Pognan F. Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur J Biochem 2000; 267: 5421-5426