Chemical constituents from the leaves and liana of Salacia nitida (Benth.) N.E.Br. (Celastraceae) and their antimicrobial activities

Subject Areas : Phytochemistry: Isolation, Purification, Characterization

Brice Mba’ning ¹ , Joël E. T. Ateba ² , Angelbert F. Awantu ³ , Luciana S. Amaral ⁴ , Gervais M. Happi ⁵ , Beate Neumann ⁶ , Georg Stammler ⁷ , Bruno Lenta ⁸ , Silvère A. Ngouela ⁹ , Iran Malavazi ¹⁰ , Etienne Tsamo ¹¹ , Norbert Sewald ¹² , Edson Rodrigues-Filho ¹³

1 - Department of Organic Chemistry, Faculty of Science, University of Yaoundé 1, Po. Box 812, Yaoundé, Cameroon
2 - Department of Organic Chemistry, Faculty of Science, University of Yaoundé 1, Po. Box 812, Yaoundé, Cameroon
3 - Department of Chemistry, Faculty of Science, University of Bamenda, Po. Box 39, Bambili, Cameroon
4 - Departamento de Química, Universidade Federal de São Carlos, CP 676, 13.565-905 SP, Brazil
5 - Department of Chemistry, Higher Teacher Training College, University of Yaoundé 1, Po. Box 47, Yaoundé, Cameroon
6 - Inorganic Chemistry, Department of Chemistry, Faculty of Chemistry, Bielefeld University, University str. 25, Bielefeld, Germany
7 - Inorganic Chemistry, Department of Chemistry, Faculty of Chemistry, Bielefeld University, University str. 25, Bielefeld, Germany
8 - Department of Chemistry, Higher Teacher Training College, University of Yaoundé 1, Po. Box 47, Yaoundé, Cameroon
9 - Department of Organic Chemistry, Faculty of Science, University of Yaoundé 1, Po. Box 812, Yaoundé, Cameroon
10 - Departamento de Genética e Evolução, Universidade Federal de São Carlos, CP 676, 13.565-905 SP, Brazil
11 - Department of Organic Chemistry, Faculty of Science, University of Yaoundé 1, Po. Box 812, Yaoundé, Cameroon
12 - Department of Chemistry, Organic and Bioorganic Chemistry, Bielefeld University, Po. Box 100131, D-33501 Bielefeld, Germany
13 - Departamento de Química, Universidade Federal de São Carlos, CP 676, 13.565-905 SP, Brazil

Received: 2019-02-06 Accepted : 2019-05-16 Published : 2019-06-01

Keywords: NMR spectroscopy, <i>Salacia nitida</i> (Benth.) N.E.Br, leaves and liana, Antimicrobial Activity, benzophenone, X-ray diffraction,

Abstract :

One benzophenone, 4′-hydroxy-2,4,6-trimethoxybenzophenone (1) was isolated from the liana and leaves of Salacia nitida (Benth.) N.E.Br., together with n-hexacosane (2), 29-hydroxyfriedelane (3), 3β-friedelinol (4), n-hexacosan-1-ol (5), n-octacosan-1-ol (6), mangiferin (7), β-sitosterol-3-O-β-D-glucopyranoside (8), friedelin (9), 30-hydroxyfriedelin (10), salaspermic acid (11), 22β-epi-maytenfolic acid (12), orthosphenic acid (13), maltose (14), D-mannitol (15), cangoronine (16), 7-hydroxyfriedelane-1,3-dione (17), tingenone (18), pristimerin (19), α-amyrin acetate (20), β-sitosterol (21) and stigmasterol (22), 21-hydroxyfriedelan-3-one (23), abruslactone A (24), and 2α-hydroxypopulnonic acid (25). The structures of the isolated compounds were established by means of spectroscopic analysis. In addition, the structure of (1) was confirmed by its X-ray diffraction. Compounds (1), (7), (10)-(11), (13), (16)-(19) and (25) were evaluated for their antimicrobial activities. Compound (18) showed a significant activity against Staphylococcus aureus (MIC = 23.8 µM) while compounds (11) and (19) exhibited moderate inhibiting effect against Staphylococcus aureus (MIC = 53.8 µM) and Candida glabrata (MIC = 105.9 µM), respectively.

References:

Bankeu, K.J.J., Dawé, A., Mbiantcha, M., Feuya, T.G.R., Ali, I., Tchuenmogne, T.M.A., Mehreen, L., Lenta, N.B., Ali, M.S., Ngouela, S.A., 2017. Characterization of bioactive compounds from Ficus vallis-choudae Delile (Moraceae). Trends Phytochem. Res. 1(4), 235-242.

Basu, S., Pant, M., Rachana, R., 2013. In vitro antioxidant activity of methanolic-aqueous extract powder (root and stem) of Salacia oblonga. Int. J. Pharm. Pharm. Sci. 5(3), 904-909.

Bertil, H., Hans, F., Bo Fredholm, B., Torsten, P., Sten, V., 1973. Secondary phosphoric acid esters and their salts. Ger. Offen. 148 pp. Patent DE2240229 A1.

Carvalho, P.R.F., Silva, D.H.S., Bolzani, V.S., Furlan, M., 2005. Antioxidant quinonemethide triterpenes from Salacia campestris. Chem. Biodivers. 2(3), 367-372.

Castilho, D.G., Chaves, A.F., Xander, P., Zelanis, A., Kitano, E.S., Serrano, S.M., Tashima, A.K., Batista, W.L., 2014. Exploring potential virulence regulators in Paracoccidioides brasiliensis isolates of varying virulence through quantitative proteomics. J. Proteome Res. 13(10), 4259-4271.

Chang, H.M., Chiang, T.C., Thomas, C.W.M., 1982.Isolation and structure elucidation of abruslactone A: A new oleanene-type triterpene from the roots and vines of Abrus precatorius L. J. Chem. Soc. Chem. Commun. 20, 1197-1198.

Chaturvedula, V.S.P., Prakash, I., 2012. Isolation of stigmasterol and β-sitosterol from the dichloromethane extract of Rubus suavissimus. Int. Curr. Pharm. J. 1(9), 239-242.

Chuluunbaatar, E., Sodnomtseren, P., Chimedtseren, C., Batsuren, G., Dulamjav, B., 2017. Isolation of two flavonoids and mannitol from Lagotis integrifolia (Willd.) Schischk (Scrophulariaceae). Cent. Asian J. Med. Sci. 3(2), 167-172.

CLSI, 2008. Reference method for broth dilution antifungal. Susceptibility testing of filamentous fungi; Approved Standard-Second Edition. CLSI document M38-A2. Wayne, PA: Clinical and Laboratory Standards Institute, 28(16).

CLSI, 2015. Methods for dilution antimicrobial. Susceptibility tests for bacteria that grow aerobically; Approved Standard-Tenth Edition. CLSI document M07-A10. Wayne, PA: Clinical and Laboratory Standards Institute, 35(2).

Colson, P., Slessor, K.N., Jennings, H.J., Smith, C.P., 1975. A carbon-13 nuclear magnetic resonance study of chlorinated and polyol analogs of glucose and related oligomers. Can. J. Chem. 53(7), 1030-1037.

Cos, P., Vlietinck, A.J., Berghe, D.V., Maes, L., 2006. Anti-infective potential of natural products: How to develop a stronger in vitro ‘proof-of-concept’. J. Ethnopharmacol. 106, 290-302.

De Mello, S.S., Tyne, D.V., Dabul, A.N.G., Gilmore, M.S., Camargo, I.L.B.C., 2016. High-quality draft genome sequence of the multidrug-resistant clinical isolate Enterococcus faecium VRE16. Genome Announc. 4(5), e00992-16.

Deepak, K.G.K., Giri, P.R., Kishor, P.B.K., Suekha, C., 2015. Salacia as an ayurvedic medicine with multiple targets in diabetes and obesity. Ann. Phytomed. 4(1), 46-53.

Dikaso, D., Makonnen, E., Debella, A., Abede, D., Urga, K., Makonnen, W., Melaku, D., Assefa, A., Makonnen, Y., 2006. In vitro anti-malarial activity of hydroalcoholic extracts from Asparagus africanus Lam in mice infected with P. bergei. Ethiop. J. Health Dev. 20(2), 117-121.

Dolomanov, O.V., Bourhis, L.J., Gildea, R.J., Howard, J.A.K., Puschmann, H., 2009. OLEX2: A complete structure solution, refinement and analysis program. J. Appl. Crystallogr. 42(2), 339-341.

Dooka, B.D., Ezejiofor, A.N, 2017. Antidiabetic and cytoprotective effects of ethanolic extract of Salacia nitida root on alloxan-induced diabetic rats. IOSR J. Pharm. Biol. Sci. 12(1), 87-93.

Duarte, L.P., Silva de Miranda, R.R., Rodrigues V.S.B., Silva, G.D.F., Vieira Filho, S.A., Knupp, V.F., 2009. Stereochemistry of 16α-hydroxyfriedelin and 3-oxo-16-methylfriedel-16-ene established by 2D NMR spectroscopy. Molecules 14, 598-607.

El-seedi, H.R, El-Barbary, M.A., El-Ghorab, D.M.H., Bohlin, L., Borg-Karlson, A.-K., Goransson, U., Verpoorte, R., 2010. Recent insights into the biosynthesis and biological activities of natural xanthones. Curr. Med. Chem. 17, 854-901.

Elujoba, A.A., Odeleye, O.M., Ogunyemi, C.M., 2005. Traditional medicine development for medical and dental primary health care delivery systems in Africa. Afr. J. Trad. Complement. Altern. Med. 21(1), 46-61.

Estrada, R., Cardenas, J., Esquivel, B., Rodriguez-Hahn, L., 1994. D:A-Friedo-oleanane triterpenes from the roots of Acanthothamnus aphyllus. Phytochemistry 36(3), 747-751.

Ezem, S.N., Akpuaka, M.U., Ajiwe, V.I.E., 2015. Isolation of quinomethides-tingenone and pristimerin from the whole root of Salacia oliveriana (Celastraceae). American J. Chem. Appl. 2(6), 120-128.

Ganesan, K., Xu, B., 2017. Ethnobotanical studies on folkloric medicinal plants in Nainamalai, Namakkal District, Tamil Nadu, India. Trends Phytochem. Res. 1(3), 153-168.

Gohil, V.M., Sheth, S.A., Nilsson, R., Wojtovich, A.P., Lee, J.H., Perocchi, F., Chen, W., Clish, C., Ayata, C., Brookes, P.S., Mootha, V.K., 2010. Nutrient-sensitized screening for drugs that shift energy metabolism from mitochondrial respiration to glycolysis. Nat. Biotechnol.28(3), 249-257.

Gunatilaka, A.A.L., Fernando, C., Kikuchi, T., Tezuka, Y., 1989. ¹H and ¹³C NMR analysis of three quinone-methide triterpenoids. Magn. Reson. Chem. 27, 803-811.

Hallé, N., 1990. Célastracées (Hippocratéoïdées), in: MESIRES (Ed.), Flore du Cameroun 32. MESIRES, Yaoundé, Cameroun, pp 110-111.

Hu, P.-Y., Zhang, D., Pu, S.-B., Li, Z.-L., Zhou, H.-H., 2014. Chemical constituents from the roots of Tripterygium wilfordii. Asian J. Chem. 26(14), 4344-4346.

Itokawa, H., Shirota, O., Ikuta, H., Morita, H., Takeya, K., Iitaka, Y., 1991. Triterpenes from Maytenus ilicifolia. Phytochemistry 30(11), 3713-3716.

Joshi, B.S., Kamat, V.N., Viswanat, N., 1973. Triterpenes of Salacia prinoides DC. Tetrahedron 29(10), 1365-1374.

Kainsa, S., Singh, R., 2016. Flavan-3-ol isomers isolated from Euphorbia thymifolia. Pharmacogn. Commun. 6(1), 28-33.

Karunanayake, E.H., Sirimanne, S.R., 1985. Mangiferin from the root barks of Salacia reticulata. J. Ethnopharmacol. 13(2), 227-228.

Kawazoe, K., Shimogni, N., Takaishi, Y., Rao, K.S., Imakura, Y., 1997. Four stilbenes from Salacia lehmbachii. Phytochemistry 44(8), 1569-1573.

Kim, C.Y., Mi-Jeong, A., Kim, J., 2006. Preparative isolation of mangiferin from Anemarrhena asphodeloides rhizomes by centrifugal partition chromatography. J. Liq. Chromatogr. Relat. Technol. 29, 869-875.

Kishi, A., Morikawa, T., Matsuda, H., Yoshikawa, M., 2003. Structures of new friedelane- and norfriedelan-type triterpenes and polyacylated eudesmane-type sesquiterpene from Salacia chinensis Linn. (S. prinoides DC., Hippocrateaceae) and radical scavenging activities of principal constituents. Chem. Pharm. Bull. 51 (9), 1051-1055.

Mba’ning, B.M., Lenta, B.N., Ngouela, S., Noungoue, D.T., Tantangmo, F., Talontsi, F.M., Tsamo, E., Laatsch, H., 2011. Salacetal, an oleanane-type triterpene from Salacia longipes var. camerunensis. Z. Naturfforsch. 66b, 1270-1274.

Mohammadhosseini, M., Sarker, S.D., Akbarzadeh, A., 2017. Chemical composition of the essential oils and extracts of Achillea species and their biological activities: A review. J. Ethnopharmacol. 199, 257-315.

Nwiloh, B.I., Uwakwe, A.A., Akaninwor, J.O., 2016. Phytochemical screening and GC-FID analysis of ethanolic extract of root bark of Salacia nitida L. Benth. J. Med. Plants Stud. 4(6), 283-287.

Nwiloh, B.I., Uwakwe, A.A., Akaninwor, J.O., 2019. Biochemical effects of ethanolic extract from root bark of Salacia nitida L. Benth in Plasmodium berghei-malaria-infected mice. A. J. Physiol. Biochem. Pharmacol. 9(1), 1-8.

Ogbonna, D.N., Sokari, T.G., Agomuoh, A.A., 2008. Antimalarial activity of some selected traditional herbs from South Eastern Nigeria against Plasmodium species. Res. J. Parasitol. 3(1), 25-31.

Okoye, N.N., Ajaghaku, D.L., Okeke, H.N., Ilodigwe, E.E., Nworu, C.S., Okoye, F.B.C., 2014. Beta-amyrin and alpha-amyrin acetate isolated from the stem bark of Alstonia boonei display profound anti-inflammatory activity. Pharm. Biol. 52(11), 1478-1486.

Patra, A., Chaudhuri, S.K., 1987. Assignment of carbon-13 nuclear magnetic resonance spectra of some friedelanes. Magn. Reson. Chem. 25(2), 95-100.

Perruchon, S., 2004. Synthèses et étude des relations structure-fonction des flavonoides. Thèse de Doctorat, Université de Rennes 1, Rennes, France, P.139.

Peshin, T., Kar, H.K., 2017. Isolation and characterization of β-sitosterol-3-O-β-D-glucoside from the extract of the flowers of Viola odorata. Br. J. Pharm. Res. 16(4), 1-8.

Rodrigues, V.G., Duarte, L.P., Silva, G.D.F., Silva, F.C., Góes, J.V., Takahashi, J.A., Pimenta, L.P.S., 2012. Evaluation of antimicrobial activity and toxic potential of extracts and triterpenes isolated from Maytenus imbricata. Quim. Nova 35(7), 1375-1380.

Rukaiyat, M., Garba, S., Labaran, S., 2015. Antimicrobial activities of hexacosane isolated from Sanseveria liberica (Gerome and Labroy) plant. Adv. Med. Plant Res. 3(3), 120-125.

Sellamuthu, P.S., Arulselvan, P., Munappan, B.P., Kandasamy, M., 2012. Effect of mangiferin isolated from Salacia chinensis regulates the kidney carbohydrate metabolism in streptozotocin-induced diabetic rats. Asian Pac. J. Trop. Biomed. 2(3), S1583-S1587.

Setzer, W.N., Setzer, M.C., Peppers, R.L., McFerrin, M.B., Meehan, E.J., Chen, L., Bates, R.B., Nakkiew, P., Jackes, B.R., 2000. Triterpenoid constituents in the bark of Balanops australiana. Australian J. Chem. 53(9), 809-812.

Sheldrick, G.M., 2008. A short history of SHELX. Acta Crystallogr. A 64(1), 112-122.

Sheldrick, G.M., 2015. Cristal structure refinement with SHELXL. Acta Crystallogr. C Struc. Chem. 71(1), 3-8.

Silva, G.D.F., Duarte, L.P., Vieira Filho, S.A., Doriguetto, A.C., Mascarenhas, Y.P., Ellena, J., Castellano, E.E., Cota, A.B., 2002. Epikatonic acid from Austroplenckia populnea: structure elucidation by 2D NMR spectroscopy and X-ray crystallography. Magn. Reson. Chem. 40(5), 366-370.

Singh, A.K., Raj, V., Keshari, A.K., Rai, A., Kumar, P., Rawat, A., Maity, B., Kumar, D., Prakask, A., De, A., Samanta, A., Bhattacharya, B., Saha, S., 2018. Isolated mangiferin and naringerin exert antidiabetic effect via PPAR_Y/GLUT4 dual agonistic action with strong metabolic regulation. Chem. Biol. Interact. 25, 280:33-44.

Thippeswamy, G., Sheela, M.L., Salimath, B.P., 2008. Octacosanol isolated from Tinospora cardifolia downregulates VEGF gene expression by inhibiting nuclear translocation of NFB and its DNA binding activity. Eur. J. Pharmacol. 588(2-3), 141-150.

Warrier, P.K., Nambiar, V.P.K., Ramankutty, C., 1994. Indian Medicinal Plants - A Compendium of 500 Species, Orient Longman Private Ltd.: 3-6-752, Himayatnagar, Hyderabad 500 029 (A.P.), India, p 47.

Zawua, C.I., Kagbo, H.D., 2018. Anti-diabetic properties of the root extracts of Salacia nitida Benth on alloxan induced diabetic rats. European J. Med. Plants 24(3), 1-15.