Phytochemical study and anti-inflammatory activity of the roots of Mangifera indica L. in lipopolysaccharide (LPS)-stimulated peritoneal macrophages

Document Type: Original Article

Authors

1 Department of Chemistry, Faculty of Sciences, P.O. Box 24157, University of Douala, Cameroon

2 Department of Physical and Analytical Chemistry, University of Jaén, Campus Las Lagunillas S/N, E-23071 Jaén, Spain

3 Department of Animal Biology, Faculty of Sciences, P.O. Box 67, University of Dschang, Cameroon

4 Department of Animal Biology and Physiology, Faculty of Sciences, P.O. Box 24157, University of Douala, Cameroon

Abstract

This study deals with the identification of secondary metabolites of methanol extract of the roots of Mangifera indica L and the assessment of plant in vitro anti-inflammatory activity. High-performance liquid chromatography with electrospray ionization mass spectrometric detection (HPLC-ESI-MSn) using the negative ion mode was performed to establish the chromatographic fingerprint and identify various chemical components of the plant extract. The anti-inflammatory effect of the MeOH extract (3, 30 and 300 μg/mL) was assessed through cell viability and nitric oxide (NO) production on non-stimulated and LPS-stimulated peritoneal macrophages. Phytochemical analysis indicated the presence of a number of phenolic compounds where galloyl derivatives, mangiferin and its derivatives were the major constituents. The methanol extract exhibited significant concentration-dependent inhibitory effect on NO production, both on stimulated and non-stimulated macrophages. The concentration 300 μg/mL showed significant cell toxicity. The methanol extract of Mangifera indica is rich in phenolic compounds and possesses potent in vitro anti-inflammatory activity, but its higher concentrations are cytotoxic.

Graphical Abstract

Phytochemical study and anti-inflammatory activity of the roots of Mangifera indica L. in lipopolysaccharide (LPS)-stimulated peritoneal macrophages

Keywords


Aderibigbe, A.O., Emudianughe, T.S., Lawal, B.A., 1999. Antihyperglycaemic effect of Mangifera indica in rat. Phytother. Res. 13, 504-507.

Barreto, J.C., Trevisan, M.T.S., Hull. W.E., Erben, G., de Brito, E.S., Pfundstein, B., Würtele, G., Spiegelhalder, B., Owen, R.W., 2008. Characterization and quantitation of polyphenolic compounds in bark, kernel, leaves, and peel of Mango (Mangifera indica L.). J. Agric. Food Chem. 56, 5599-5610.

Baskaran, A., Chua, K.H., Sabaratnam, V., Ram, R.M., Kuppusamy, U.R., 2017. Pleurotus giganteus (Berk. Karun & Hyde), the giant oyster mushroom inhibits NO production in LPS/H2O2 stimulated RAW 264.7 cells via STAT 3 and COX-2 pathways. BMC Complement. Altern. Med. 17, 1-10. DOI 10.1186/s12906-016-1546-6

Boscá, L., Zeini, M., Través, P.G., Hortelano, S., 2005. Nitric oxide and cell viability in inflammatory cells: a role for NO in macrophage function and fate. Toxicology 208, 249-258.

Bulugonda, R.K., Kumar, K.A., Gangappa, D., Beeda, H., Philip, G.H., Rao, D.M., Faisal, S.M., 2017. Mangiferin from Puerariatuberosa reduces inflammation via inactivation of NLRP3 inflammasome. Sci. Rep. 7, DOI: 10.1038/srep42683

Cheng, B.C.Y., Ma, X.Q., Kwan, H.Y., Tse, K.W., Cao, H.H., Su, T., Shu. X., Wu, Z.Z., Yu, Z.L. 2014. A herbal formula consisting of Rosae Multiflorae Fructus and Lonicerae Japonicae Flos inhibits inflammatory mediators in LPS-stimulated RAW264.7 macrophages. J. Ethnopharmacol. 153, 922-927.

Cuschieri, J., Maier, R.V., 2007. Oxidative stress, lipid rafts, and macrophage reprogramming. Antioxid. Redox Signal. 9, 1485-1498.

Dorta, E., González, M., Lobo, M.G., Sánchez-Moreno, C., de Ancos, B., 2014. Screening of phenolic compounds in by-product extracts from mangoes (Mangifera indica L.) by HPLC-ESI-QTOF-MS and multivariate analysis for use as a food ingredient. Food Res. Int. 57, 51-60.

Farnsworth, N.R., Soejarto, D.D., 1991. Global importance of medicinal plants. In: Akerele, O., Heywood, V., Synge, H. (Eds.), Conservation of Medicinal Plants. Cambridge University Press, Cambridge, pp. 25-51.

Förstermann, U., 2010. Nitric oxide and oxidative stress in vascular disease. Pflug. Arch. Eur. J. Phy. 459, 923-939.

Frezza, C., Venditti, A., Serafini, I., Carassiti, A., Foddai, S., Bianco, A., Serafini, M., 2017. Phytochemical characteristics of Galeopsis ladanum subsp. angustifolia (Ehrh. ex Hoffm.) Gaudin collected in Abruzzo region (Central Italy) with chemotaxonomic and ethnopharmacological implications. Trends Phytochem. Res. 1(2), 61-68.

Garrido, G., González, D., Delporte, C., 2001. Analgesic and anti-inflammatory effects of Mangifera indica extract (Vimang). Phytother. Res. 15, 18-21.

Garrido, G., Gonzalez, D., Lemus, Y., Delporte, C., Delgado, R., 2006. Protective effects of a standard extract of Mangifera indica L. (VIMANG) against mouse ear edemas and its inhibition of eicosanoid production in J774 murine macrophages. Phytomedicine 13, 412-418.

Gómez-Caravaca, A.M., López-Cobo, A., Verardo, V., Segura-Carretero, A., Fernández-Gutiérrez, A., 2016. HPLC-DAD-q-TOF-MS as a powerful platform for the determination of phenolic and other polar compounds in the edible part of mango and its by-products (peel, seed, and seed husk). Electrophoresis 37, 1072-1084.

Justesen, U., 2000. Negative atmospheric pressure chemical ionisation low-energy collision activation mass spectrometry for the characterisation of flavonoids in extracts of fresh herbs. J. Chromatogr. A 902, 369-379.

Kanwal, Q., Hussain, I., Siddiqui, H.L., Javaid, A., 2010. Antifungal activity of flavonoids isolated from mango (Mangifera indica L.) leaves. Nat. Prod. Res. 24, 1907-1914.

Llorent-Martínez, E.J., Zengin, G., Lobine, D., Molina-García, L., Mollica, A., Mahomoodally, M.F., 2018. Phytochemical characterization, in vitro and in silico approaches for three Hypericum species. New J. Chem. 42, 5204-5214.

Lucas, K., Maes, M., 2013. Role of the Toll Like receptor (TLR) radical cycle in chronic inflammation: Possible treatments targeting the TLR4 pathway. Mol. Neurobiol. 48, 190-204.

Magne, F.A.L., Nguemfo, E.L., Djouatsa Nangue, Y., Bogning, Z.C., Fouokeng, Y., Azebaze, A.G.B., Llorent-Martínez, J.E., Fernández-de Córdova, M.L., Dongmo, A.B., Vierling, W., 2017. Antinociceptive and anti-inflammatory effects of the methanolic stem bark extract of Antrocaryon klaineanum Pierre (Anacardiaceae) in mice and rat. J. Ethnopharmacol. 203, 11-19.

Mämmelä, P., 2001. Phenolics in selected European hardwood species by liquid chromatography-electrospray ionisation mass spectrometry. Analyst 126, 1535-1538.

Marles, M.A.S., Gruber, M.Y., Scoles, G.J., Muir, A.D. 2003. Pigmentation in the developing seed coat and seedling leaves of Brassica carinata is controlled at the dihydroflavonol reductase locus. Phytochemistry 62, 663-672.

Masibo, M., He, Q., 2008. Major Mango Polyphenols and their potential significance to human health. Compr. Rev. Food Sci. Food Saf. 7, 309-319.

Mohammadhosseini, M., 2017. The ethnobotanical, phytochemical and pharmacological properties and medicinal applications of essential oils and extracts of different Ziziphora species. Ind. Crops Prod. 105, 164-192.

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.

Mohammadhosseini, M., Venditti, A., Sarker, S.D., Nahar, L., Akbarzadeh, A., 2019. The genus Ferula: Ethnobotany, phytochemistry and bioactivities - A review. Ind. Crops Prod. 129, 350-394.

Pardo-Andreu, G.L., Sanchez-Baldoquín, C., Avila-González, R., Yamamoto, E.T., Revilla, A., Uyemura, S.A., 2006. Interaction of Vimang (Mangifera indica L. extract) with Fe(III) improves its antioxidant and cytoprotecting activity. Pharmacol. Res. 54, 389-395.

Park, K.H., Yoon, K.H., Yin, J., Le, T.T., Ahn, H.S., Yoon, S.H., Lee, M.W., 2017. Antioxidative and anti-inflammatory activities of galloyl derivatives and antidiabetic activities of Acer ginnala. Evid. Based Complement. Alternat. Med. http://dx.doi.org/10.1155/2017/6945912

Prasad, S., Kalra, N., Shukla, Y., 2007. Hepatoprotective effects of lupeol and mango pulp extract of carcinogen induced alteration in Swiss albino mice. Mol. Nutr. Food Res. 51, 352-359.

Rocha Ribeiro, S.M., Queiroz, J.H., Lopes Ribeiro, M.E., Campos, F.M., Pinheiro Santana, H.M., 2007. Antioxidant in mango (Mangifera indica L.) pulp. Plant Foods Hum. Nutr. 62, 13-17.

Sánchez, G.M., Re, L., Giuliani, A., Núñez-Sellésd, A.J., Davisona, G.P., León-Fernández, O.S., 2000. Protective effects of Mangifera indica L. extract mangiferin and selected anti-oxidants against TPAinduced biomolecules oxidation and peritoneal macrophage activation in mice. Pharm. Res. 42, 565-573.

Scartezzini, P., Speroni, E., 2000. Review on some plants of Indian traditional medicine with antioxidant activity. J. Ethnopharmacol. 71, 23-43.

Sharma, S.R., Dwivedi, S.K., Swarup, D. 1997. Hypoglycemic potential of Mangifera indica leaves in rats. Int. J. Pharm. 35, 130-133.

Shaw, C.A., Taylor, E.L., Megson, I.L., Rossi, A.G., 2005. Nitric oxide and the resolution of inflammation: implications for atherosclerosis. Mem. Inst. Oswaldo Cruz 100, 67-71.

Shu, M., Hu, X.R., Hung, Z.A., Huang, D.D., Zhang, S., 2016. Effects of tanshinone IIA on fibrosis in a rat model of cirrhosis through heme oxygenase-1, inflammation, oxidative stress and apoptosis. Mol. Med. Rep. 13, 3036-3042.

Sosa, S., Balick, M.J., Arvigo, R., Esposito, R.G., Pizza, C., Altinier, G., Tubaro, A., 2002. Screening of the topical anti-inflammatory activity of some Central American plants. J. Ethnopharmacol. 81, 211-215.

Sun, J., Liang, F., Bin, Y., Li, P., Duan, C., 2007. Screening non-colored phenolics in red wines using liquid chromatography/ultraviolet and mass spectrometry/mass spectrometry libraries. Molecules 12, 679-693.

Verardo, G., Duse, I., Callea, A., 2009. Analysis of underivatized oligosaccharides by liquid chromatography/electrospray ionization tandem mass spectrometry with post-column addition of formic acid. Rapid Commun. Mass Spectrom. 23, 1607-1618.

Vyas, A., Syeda, K., Ahmad, A., Padhye, S.H., Sarkar, F., 2012. Perspectives on medicinal properties of mangiferin. Mini. Rev. Med. Chem. 12, 412-425.

Wang, J., Mazza, G., 2002. Inhibitory effects of anthocyanins and other phenolic compounds on nitric oxide production in LPS/IFN--activated RAW 264.7 macrophages. J. Agric. Food Chem. 50, 850-857.

Ye, M., Yang, W.Z., Liu, K.D., Qiao, X., Li, B.J., Cheng, J., Feng, J., Guo, D.A., Zhao, Y.Y., 2012. Characterization of flavonoids in Millettia nitida var. hirsutissima by HPLC/DAD/ESI-MSn. J. Pharm. Anal. 2, 35-42.