Generic placeholder image

Current Pharmaceutical Biotechnology

Author(s): Hala S. Mohammed, Marwa M. Abdel-Aziz, Marwa S. Abu-Baker, Amal M. Saad, Mona A. Mohamed and Mosad A. Ghareeb*

DOI: 10.2174/1389201020666190613161212

DownloadDownload PDF Flyer Cite As
Antibacterial and Potential Antidiabetic Activities of Flavone C-glycosides Isolated from Beta vulgaris Subspecies cicla L. var. Flavescens (Amaranthaceae) Cultivated in Egypt

Page: [595 - 604] Pages: 10

  • * (Excluding Mailing and Handling)

Abstract

Background: Diabetes mellitus is the most common disease in Egypt. In this context, Beta vulgaris subspecies cicla L. var. flavescens is an edible plant that has been used in traditional medicine as a therapy for treating some diseases.

Objectives: The current study was performed to evaluate the antibacterial and potential anti-diabetic activities of different extracts and isolated flavone C-glycoside compounds isolated from Beta vulgaris subspecies cicla L. var. flavescens leaves.

Methods: Phytochemical investigation of n-butanol extract led to the isolation of five phytoconstituents. Their structures were determined by spectroscopic tools, including 1D-NMR (1H- & 13C-NMR) and 2D-NMR (HMQC & HMBC) besides the comparison of the data with the literature. The extracts and phytoconstituents were evaluated in vitro for their activity against some bacterial pathogens, which represent prominent human pathogens, particularly in hospital settings. The antibacterial activity was examined against three Gram-positive bacterial strains (Staphylococcus aureus, Staphylococcus epidermidis & Enterococcus faecalis) and five Gram-negative ones (Pseudomonas aeruginosa, Proteus vulgaris, Klebsiella pneumoniae, Proteus mirabilis & Salmonella typhimurium) relative to Ciprofloxacin as a reference drug. Furthermore, the in vitro antidiabetic activity (Type II) was evaluated using the alpha-glucosidase inhibitory assay.

Results: Five flavone C-glycosides namely; Apigenin 8-C-β-D-glucopyranoside (vitexin) (1), 2''-Oxylopyranosylvitexin (2), acacetin 8-C-β-D-glucopyranoside (3), acacetin 8-C-α-L-rhamnoside (4), and 6,8-di-C-β-D-glucopyranosylapigenin (vecinin-II) (5) were isolated from n-butanol extract of B. vulgaris subspecies cicla L. var. flavescens. Compound 1 showed a promising antibacterial activity against most of the test bacterial strains with respect to the minimum inhibitory concentration values (MIC) ranged from 1.95 to 15.63 µg ml-1. On the other hand, compounds 1 and 3 demonstrated superior antidiabetic activities with IC50 values of 35.7 and 42.64 µg ml-1, respectively, while an inferior potential antidiabetic activity was recorded for compound 4 (IC50 = 145.5 µg ml-1) in comparison with Acarbose as a reference drug.

Conclusion: B. vulgaris L. is an edible plant, which could be used as a natural source of antibiotic and hypoglycemic drugs.

Keywords: Amaranthaceae, Beta vulgaris subspecies cicla L. var. flavescens, flavonoids, antibacterial, antidiabetic, saponins.

Graphical Abstract

[1]
Kim, Y.; Han, M.S.; Lee, J.S.; Kim, J.; Kim, Y.C. Inhibitory phenolic amides on lipopolysaccharide-induced nitric oxide production in RAW 264.7 cells from Beta vulgaris var. cicla seeds. Phytother. Res., 2003, 17(8), 983-985. [http://dx.doi.org/10.1002/ptr.1232]. [PMID: 13680842].
[2]
Kim, I.; Chin, Y.W.; Lim, S.W.; Kim, Y.C.; Kim, J. Norisoprenoids and hepatoprotective flavone glycosides from the aerial parts of Beta vulgaris var. cicla. Arch. Pharm. Res., 2004, 27(6), 600-603. [http://dx.doi.org/10.1007/BF02980156]. [PMID: 15283459].
[3]
Hashem, A.N.; Soliman, M.S.; Hamed, M.A.; Swilam, N.F.; Lindequist, U.; Nawwar, M.A. Beta vulgaris subspecies cicla var. flavescens (Swiss chard): Flavonoids, hepatoprotective and hypolipidemic activities. Pharmazie, 2016, 71(4), 227-232. [PMID: 27209705].
[4]
Yanardağ, R.; Çolak, H. Effect of chard (Beta vulgaris L. var. cicla) on blood glucose levels in normal and alloxan-induced diabetic rabbits. Pharm. Pharmacol. Commun., 1998, 4, 309-311.
[5]
Yarat, A.; Özçelik, F.; Yanardağ, R.; Tunali, T.; Özsoy, Ö.; Emekli, N. The effect of chard (Beta vulgaris L. var. cicla) on the protein and antioxidant systems in lenses of streptozotocin-induced diabetic rats. Pharm. Pharmacol. Commun., 1998, 4, 271-274.
[6]
Tunali, T.; Yarat, A.; Yanardağ, R.; Ozçelík, F.; Özsoy, O.; Ergenekon, G.; Emeklí, N. The effect of chard (Beta vulgaris L. var. cicla) on the skin of streptozotocin induced diabetic rats. Pharmazie, 1998, 53(9), 638-640. [PMID: 9770212].
[7]
Bolkent, S.; Yanardağ, R.; Tabakoğlu-Oğuz, A.; Ozsoy-Saçan, O. Effects of chard (Beta vulgaris L. var. Cicla) extract on pancreatic B cells in streptozotocin-diabetic rats: A morphological and biochemical study. J. Ethnopharmacol., 2000, 73(1-2), 251-259. [http://dx.doi.org/10.1016/S0378-8741(00)00328-7]. [PMID: 11025163].
[8]
Sener, G.; Saçan, O.; Yanardağ, R.; Ayanoğlu-Dülger, G. Effects of chard (Beta vulgaris L. var. cicla) extract on oxidative injury in the aorta and heart of streptozotocin-diabetic rats. J. Med. Food, 2002, 5(1), 37-42. [http://dx.doi.org/10.1089/109662002753723205]. [PMID: 12511111].
[9]
Yanardağ, R.; Bolkent, S.; Ozsoy-Saçan, O.; Karabulut-Bulan, O. The effects of chard (Beta vulgaris L. var. cicla) extract on the kidney tissue, serum urea and creatinine levels of diabetic rats. Phytother. Res., 2002, 16(8), 758-761. [http://dx.doi.org/10.1002/ptr.1041]. [PMID: 12458482].
[10]
Gezginci-Oktayoglu, S.; Sacan, O.; Bolkent, S.; Ipci, Y.; Kabasakal, L.; Sener, G.; Yanardag, R. Chard (Beta vulgaris L. var. cicla) extract ameliorates hyperglycemia by increasing GLUT2 through Akt2 and antioxidant defense in the liver of rats. Acta Histochem., 2014, 116(1), 32-39. [http://dx.doi.org/10.1016/j.acthis.2013.04.016]. [PMID: 23746671].
[11]
Masayuki, Y.; Shoichi, H. Extraction of blood glucose sugar lowering saponins from Beta vulgaris’, Jpn. Kokai Tokkyo Koho JP (Japan), 09 25290 (Appl. 95:177. 220, 1995), 9 pp. Chem. Abstr., 1997, 126203699c.
[12]
Dijoux, M.G.; Lavaud, C.; Massiot, G.; Lemen-Oliver, L. Flavonoids from Beta vulgaris varieties. Fitoterapia, 1995, 66, 189-195.
[13]
Gil, M.I.; Ferreres, F.; Tomás‐Barberán, F.A. Effect of modified atmosphere packaging on the flavonoids and vitamin C content of minimally processed Swiss chard (Beta vulgaris subspecies cycla). J. Agric. Food Chem., 1998, 46, 2007-2012. [http://dx.doi.org/10.1021/jf970924e].
[14]
Ninfali, P.; Bacchiocca, M.; Antonelli, A.; Biagiotti, E.; Di Gioacchino, A.M.; Piccoli, G.; Stocchi, V.; Brandi, G. Characterization and biological activity of the main flavonoids from Swiss Chard (Beta vulgaris subspecies cycla). Phytomedicine, 2007, 14(2-3), 216-221. [http://dx.doi.org/10.1016/j.phymed.2006.03.006]. [PMID: 16698256].
[15]
Ninfali, P.; Angelino, D. Nutritional and functional potential of Beta vulgaris cicla and rubra. Fitoterapia, 2013, 89, 188-199. [http://dx.doi.org/10.1016/j.fitote.2013.06.004]. [PMID: 23751216].
[16]
Kugler, F.; Stintzing, F.C.; Carle, R. Identification of betalains from petioles of differently colored Swiss chard (Beta vulgaris L. ssp. cicla [L.] Alef. Cv. Bright Lights) by high-performance liquid chromatography-electrospray ionization mass spectrometry. J. Agric. Food Chem., 2004, 52(10), 2975-2981. [http://dx.doi.org/10.1021/jf035491w]. [PMID: 15137842].
[17]
Zeller, W.; Rudolph, K.; Hoppe, H.H. Effect of the pseudomonas phaseolicolatoxin on the composition of lipids in leaves of Swiss chard. II: Changes in the fatty acid spectrum of phospholipids and glycolipids. Phytopathol. Z., 1977, 89, 296-305. [http://dx.doi.org/10.1111/j.1439-0434.1977.tb02870.x].
[18]
Snežana, T.; Ana, T.; Mirko, K.; Vlatka, V. Free radicals and antioxidants: Antioxidative and other properties of Swiss chard (Beta vulgaris L. subsp. cicla). Poljopr. Sumar., 2015, 61, 73-92.
[19]
Zein, H.; Hashish, A.S.; Ismaiel, G.H.H. The antioxidant and anticancer activities of Swiss chard and red beet root leaves. Curr. Sci. Int., 2015, 04, 491-498.
[20]
Blázovics, A.; Nyirády, P.; Romics, I.; Szűcs, M.; Horváth, A.; Szilvás, A. How can cancer-associated anemia be moderated with nutritional factors and how do Beta vulgaris L. sp; Esculenta Var, 2012.
[21]
Bandow, J.E.; Brötz, H.; Leichert, L.I.O.; Labischinski, H.; Hecker, M. Proteomic approach to understanding antibiotic action. Antimicrob. Agents Chemother., 2003, 47(3), 948-955. [http://dx.doi.org/10.1128/AAC.47.3.948-955.2003]. [PMID: 12604526].
[22]
El-Seedi, H.R.; Ohara, T.; Sata, N.; Nishiyama, S. Antimicrobial diterpenoids from Eupatorium glutinosum (Asteraceae). J. Ethnopharmacol., 2002, 81(2), 293-296. [http://dx.doi.org/10.1016/S0378-8741(02)00101-0]. [PMID: 12065166].
[23]
Parekh, J.; Chanda, S. Antibacterial and phytochemical studies on twelve species of Indian medicinal plants. Afr. J. Biol. Res, 2007, 10, 175-181.
[24]
Mbaveng, A.T.; Sandjo, L.P.; Tankeo, S.B.; Ndifor, A.R.; Pantaleon, A.; Nagdjui, B.T.; Kuete, V. Antibacterial activity of nineteen selected natural products against multi-drug resistant Gram-negative phenotypes. Springerplus, 2015, 4, 823. [http://dx.doi.org/10.1186/s40064-015-1645-8]. [PMID: 26753111].
[25]
Funke, I.; Melzig, M.F. Traditionally used plants in diabetes therapy-phytotherapeutics as inhibitors of α-amylase activity. Rev. Bras. Farmacogn., 2006, 16, 1-5. [http://dx.doi.org/10.1590/S0102-695X2006000100002].
[26]
Kim, K.Y.; Nam, K.A.; Kurihara, H.; Kim, S.M. Potent α-glucosidase inhibitors purified from the red alga Grateloupia elliptica. Phytochemistry, 2008, 69(16), 2820-2825. [http://dx.doi.org/10.1016/j.phytochem.2008.09.007]. [PMID: 18951591].
[27]
Lam, S.H.; Chen, J.M.; Kang, C.J.; Chen, C.H.; Lee, S.S. α-Glucosidase inhibitors from the seeds of Syagrus romanzoffiana. Phytochemistry, 2008, 69(5), 1173-1178. [http://dx.doi.org/10.1016/j.phytochem.2007.12.004]. [PMID: 18221760].
[28]
Perez, C.; Paul, M.; Bazerque, P. An antibiotic assay by the agar well diffusion method. Acta Biol. Med. Exp., 1990, 15, 113-115.
[29]
Nair, R.; Chanda, S. Antibacterial activity of Punica granatum in different solvents. Indian J. Pharm. Sci., 2005, 67, 239-243.
[30]
Shai, L.J.; Magano, S.R.; Lebelo, S.L.; Mogale, A.M. Inhibitory effects of five medicinal plants on rat alpha-glucosidase: Comparison with their effects on yeast alpha-glucosidase. J. Med. Plants Res., 2011, 5, 2863-2867.
[31]
Sharma, P.; Garg, P.; Dadhwal, S.; Singh, G.; Sharma, D.K.; Sharma, S. Antimicrobial activity of butanol extract of Malaxis acuminate. J. Pharm. Res., 2011, 4, 2703-2704.
[32]
Gangula, S.R.; Govada, H.; Matta, M. Phytochemical screening and inhibitory effect of n-butanol, isopropanol and water extracts leaf extracts of Sapindus saponaria Vahl on selected pathogens. Adv Appl Sci Res, 2013, 4, 463-467.
[33]
Rauha, J.P.; Remes, S.; Heinonen, M.; Hopia, A.; Kähkönen, M.; Kujala, T.; Pihlaja, K.; Vuorela, H.; Vuorela, P. Antimicrobial effects of Finnish plant extracts containing flavonoids and other phenolic compounds. Int. J. Food Microbiol., 2000, 56(1), 3-12. [http://dx.doi.org/10.1016/S0168-1605(00)00218-X]. [PMID: 10857921].
[34]
Koockak, H.; Seyyednejad, S.M.; Motamedi, H. Preliminary study on the anti-microbial activity of some medicinal plants of Khuzestan (Iran). Asian Pac. J. Trop. Med., 2010, 3, 180-184. [http://dx.doi.org/10.1016/S1995-7645(10)60004-1].
[35]
Hu, H.B.; Fan, J. Structural identification and antibacterial activity of chemical constituents of Acanthopanax brachypus Harms. Chin. Hosp. Pharm. J., 2008, 28, 1344-1347.
[36]
Li, S.H.; Zhao, Q.; Cheng, Y.; Liu, F. Antimicrobial activities of vitexin from Alsophila spinutosa. Food Res. Develop, 2013, 34(14), 4-6.
[37]
Brango-Vanegas, J.; Costa, G.M.; Ortmann, C.F.; Schenkel, E.P.; Reginatto, F.H.; Ramos, F.A.; Arévalo-Ferro, C.; Castellanos, L. Glycosylflavonoids from Cecropia pachystachya Trécul are quorum sensing inhibitors. Phytomedicine, 2014, 21(5), 670-675. [http://dx.doi.org/10.1016/j.phymed.2014.01.001]. [PMID: 24548722].
[38]
Cowan, M.M. Plant products as antimicrobial agents. Clin. Microbiol. Rev., 1999, 12(4), 564-582. [http://dx.doi.org/10.1128/CMR.12.4.564]. [PMID: 10515903].
[39]
Bylka, W.; Matlawska, I.; Pilewski, N.A. Natural flavonoids as antimicrobial agents. J. Am. Nutraceut. Assoc., 2004, 7, 24-31.
[40]
Rahman, A.A.; Moon, S.S. Antimicrobial phenolic derivatives from Dendranthema zawadskii var. latilobum Kitamura (Asteraceae). Arch. Pharm. Res., 2007, 30(11), 1374-1379. [http://dx.doi.org/10.1007/BF02977359]. [PMID: 18087803].
[41]
Ayaz, F.; Ayaz, H.S.; Karaoglu, S.A.; Gruz, J.; Valentová, K.; Ulrichová, J. Phenolic acid contents of kale (Brassica oleraceae L. var. acephala DC.) extracts and their antioxidant and antibacterial activities. Food Chem., 2008, 107, 19-25. [http://dx.doi.org/10.1016/j.foodchem.2007.07.003].
[42]
Rand, R.H.; Abdulamir, A.S.; Law, S.V.; Fatimah, A.B.; Faridah, A.F.; Jahanshiri, A.B.; Zamberi, S. Novel in-vitro antimicrobial activity of Vignara diata (L.) R. Wilczek against highly resistant bacterial and fungal pathogens. J. Med. Plants Res., 2011, 5(16), 3606-3618.
[43]
Sae-tan, S.; Saeting, O. Anti-diabetic activities of vitexin and isovitexin from mung bean soup. 2017.10th World Congress on Nutrition and Food Sciences, May 29-31, 2017Osaka, Japan
[44]
Chen, Y.G.; Li, P.; Li, P.; Yan, R.; Zhang, X.Q.; Wang, Y.; Zhang, X.T.; Ye, W.C.; Zhang, Q.W. α-Glucosidase inhibitory effect and simultaneous quantification of three major flavonoid glycosides in Microctis folium. Molecules, 2013, 18(4), 4221-4232. [http://dx.doi.org/10.3390/molecules18044221]. [PMID: 23612474].
[45]
Caristi, C.; Bellocco, E.; Gargiulli, C.; Toscano, G.; Leuzzi, U. Flavone-di-C-glycosides in citrus juices from Southern Italy. Food Chem., 2006, 95, 431-437. [http://dx.doi.org/10.1016/j.foodchem.2005.01.031].
[46]
Orhan, D.D.; Ozçelik, B.; Özgen, S.; Ergun, F. Antibacterial, antifungal, and antiviral activities of some flavonoids. Microbiol. Res., 2010, 165(6), 496-504. [http://dx.doi.org/10.1016/j.micres.2009.09.002]. [PMID: 19840899].
[47]
Mabry, T.J.; Markham, K.R.; Thomas, M.B. The systematic identification of flavonoids. In the Ultraviolet Spectra of Flavones and Flavonols; Springer, 1970, pp. 41-164. [http://dx.doi.org/10.1007/978-3-642-88458-0]
[48]
Harborne, J.B.; Mabry, T.J. The flavonoids In: Advances Research; 1st ed.; Springer US., 1982.
[49]
P.K, Agrawal. Carbon-13 NMR of Flavonoids., 1st ed.; Elsevier Science: Amsterdam. 1989.
[50]
Gil, M.I.; Ferreres, F. Tomas-Barberan; Francisco, A. Effect of modified atmosphere packaging on the flavonoids and vitamin C content of minimally processed Swiss Chard (Beta vulgaris subspecies Cycla). J. Agric. Food Chem., 1998, 46(5), 2007-2012. [http://dx.doi.org/10.1021/jf970924e].
[51]
Isolation and Identification of Flavonoids Found in Zostera marina Collected in Norwegian Coastal Waters. In: Techniques of Flavonoid Identification; Markham, K.R.,, Ed.; Academic Press, London. 1982. Vol. 52