Anti-melanogenic, antioxidant potentialities and metabolome classification of six Ocimum species: Metabolomics and in-silico approaches

Subject Areas : Analytical Assessments of Bioactive Compounds

Sreerupa Sarkar ¹ (Phytochemistry and Pharmacognosy Laboratory, Department of Botany, University of Calcutta, 35, Ballygunge Circular Road, Kolkata-700019)
Muddasar Hoda ² (Department of Biological Sciences, Aliah University, Newtown Campus, Kolkata-700160)
Susmita Das ³ (Phytochemistry and Pharmacognosy Laboratory, Department of Botany, University of Calcutta, 35, Ballygunge Circular Road, Kolkata-700019)

Received: 2023-01-13 Accepted : 2023-03-27 Published : 2023-03-01

Keywords: Anti-melanogenic, <i>p</i>-Arbutin, Ocimum, Antioxidant, Quinic acid, Metabolome,

Abstract :

This investigation was designed to evaluate the anti-tyrosinase and antioxidant potentialities of leaves and inflorescences of six Ocimum species. Currently, cosmaceutical and nutraceutical industries are looking for sources that are substitutes for synthetic agents which are natural or plant-derived bioactive components which are non-toxic skin lightening agents and anti-browning agents for fruits and vegetables. Both leaves and inflorescences of all the Ocimum species demonstrated anti-tyrosinase activities in a dose-dependent manner. GC/MS revealed seven phenolic compounds viz., p-arbutin, quinic acid, ferulic acid, 1,2,4-benzene triol, gallic acid, vanillic acid, and p-coumaric acid present in the studied plant parts and exhibited anti-tyrosinase activity with significant IC50 values. Metabolomic and chemometric strategies deciphered metabolome classification of the studied species. Seven identified phenolic compounds showing anti-tyrosinase activity were further subjected to in silico analysis to explore their binding mechanism with tyrosinase enzyme, and were found to interact with the targeted enzyme with high binding affinity.

References:

Afolabi, C., Akinmoladun, E., Ibukun, O., Emmanuel, A., Obuotor, E.M., Farombi, E.O., 2007. Phytochemical constituent and antioxidant activity of extract from the leaves of Ocimum gratissimum. Sci. Res. Essay. 2 (5), 163-166.
Amirahmadi, A., Naderi, R., Afsharian, M.H., 2022. An investigation into the medicinal plants of Semnan province with taxonomic and therapeutic aspects. Trends Phytochem. Res. 6(4), 312-338.
Ashraf, Z., Rafiq, M., Seo, S.Y., Babar, M.M., Sahar, N.U., Zaidi, S., 2015. Synthesis, kinetic mechanism and docking studies of vanillin derivatives as inhibitors of mushroom tyrosinase. Bioorg. Med. Chem. 23, 5870-5880.
Banerjee, A., De, B., 2013. Comparative study of antioxidant activity of the food flowers of West Bengal, India. Intl. J. Food Prop. 16, 193-204.
Barlow, S.M., 1990. Toxicological aspects of antioxidants used as food additives. Food Antioxid. 253-307.
Beauchamp, C., Fridovich, I., 1971. Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Anal Biochem. 44(1), 276-287.
Boissy, R.E., Visscher, M., DeLong, M.A., 2005. Deoxyarbutin: A novel reversible tyrosinase inhibitor with effective in vivo skin lightening potency. Exp. Dermatol. 14, 601-608.
Braca, A., Tommasi, Nunziatina, D.B., Lorenzo, D., Cosimo, P., Politi, M., Morelli, I., 2001. Antioxidant principles from Bauhinia terapotensis. J. Nat. Prod. 64, 892-895.
Brown, D.A., 2001. Skin pigmentation enhancers. J. Photochem. Photobiol. B, Biol. 63, 148-161. 
Cestari, T.F., Dantas, L.P., Boza, J.C., 2014. Acquired hyperpigmentations. An. Bras. Dermatol. 89, 11-25.
Chan, E.W.C., Lim, Y.Y., Wong, L.F., Lianto, F.S., Wong, S.K., Lim, K.K., Joe, C.E., Lim, T.Y., 2008. Antioxidant and tyrosinase inhibition properties of leaves and rhizomes of ginger species. Food Chem. 109, 477-483.
Chang, T.S., 2009. An updated review of tyrosinase inhibitors. Int. J. Mol. Sci. 10, 2440-2475.
Chawla, S., DeLong, M.A., Visscher, M.O., 2008. Mechanism of tyrosinase inhibition by deoxyarbutin and its second-generation derivatives. Br. J. Dermatol. 159, 1267-74.
Chawla, S., Kvalnes, K., DeLong, M.A., Wickett, R., Manga, P., Boissy, R.E., 2012. Deoxyarbutin and its derivatives inhibit tyrosinase activity and melanin synthesis without inducing reactive oxygen species or apoptosis. J. Drugs Dermatol. 11, e28- e34.
Chen, Y.R., Chiou, R. Y.Y., Lin, T.Y., Huang, C.P., Tang, W.C., Chen, S.T., Lin, S.B., 2009. Identification of an alkylhydroquinone from Rhus succedanea as an inhibitor of tyrosinase and melanogenesis. J. Agric. Food Chem. 57, 2200-2205.
Colquitt, R.B., Colquhoun, D.A., Thiele, R.H., 2011. In silico modelling of physiologic systems. Best Pract. Res. Clin. Anaesthesiol. 25, 499-510.
Das, S., Dutta, M., Choudhury, K., De, B., 2016. Metabolomic and chemometric study of Achras sapota L. fruit extracts for identification of metabolites contributing to the inhibition of α-amylase and α-glucosidase. Eur. Food Res. Technol. 242, 733-743.
Dorga, S., Sarangal, R., 2014. Pigmentary disorders: An insight. Pigment Int. 1, 5-7.
Ekins, S., Mestres, J., Testa, B., 2007. In silico pharmacology for drug discovery: Applications to targets and beyond. Br. J. Pharmacol. 152, 21-37.
Fiehn, O., 2006. Metabolite profiling in arabidopsis. Arabidopsis Protocols, 439-447.
Friedman, M., 1996. Food browning and its prevention: An overview. J. Agric. Food Chem. 44, 631-653.
Hashimoto, A., Ichihashi, M., Mishima, Y., 1984. The mechanism of depigmentation by hydroquinone: a study on suppression and recovery processes of tyrosinase activity in the pigment cells in vivo and in vitro. Jap. J. Dermatol. 94, 797-804.
Hearing, V.J., Tsukamoto, K., 1991. Enzymatic control of pigmentation in mammals. FASEB J. 5, 2902-2909.
Heo, S.J., Ko, S.C., Cha, S.H., Kang, D.H., Park, H.S., Choi, Y.U., Kim, D., Jung, W.K., Jeon, Y.J., 2009. Effect of phlorotannins isolated from Ecklonia cava on melanogenesis and their protective effect against photo-oxidative stress induced by UV-B radiation. Toxicol. In Vitro. 23, 1123-1130.
Kang, H.S., Kim, H.R., Byun, D.S., Son, B.W., Nam, T.J., Choi, J.S., 2004. Tyrosinase inhibitors isolated from the edible brown alga Ecklonia stolonifera. AAPS Adv. Pharm. Sci. Ser. 27, 1226-1232.
Kim, D., Jeong, S.W., Lee, C.Y., 2003. Antioxidant capacity of phenolic phytochemicals from various cultivars of plum. Food Chem. 81, 321 326.
Kim, Y.J., Kang, K.S., Yokozawa, T., 2008. The anti-melanogenic effect of pycnogenol by its anti-oxidative actions. Food Chem. Toxicol. 46, 2466-2471.
Kind, T., Wohlgemuth, G., Lee, D.Y., Lu, Y., Palazoglu, M., Sevini, S., Fiehn, O., 2009. FiehnLib-mass spectral and retention index libraries for metabolomics based on quadrupole and time-of-flight gas chromatography/mass spectrometry. Anal. Chem. 81, 10038-10048.
Kolbe, L., Mann, T., Gerwat, W., Batzer, J., Ahlheit, S., Scherner, C., Wenck, H., Stäb, F., 2013. 4-n-Butylresorcinol, a highly effective tyrosinase inhibitor for the topical treatment of hyperpigmentation. J. Eur. Acad Dermatol. Venereol. 27, 19-23.
Kunsch, C., Medford, R. M., 1995. Oxidative stress as a regulator of gene expression in the vasculature. Circ. Res. 85, 753-766.
Martinez, M.V., Whitaker, J.R., 1995. The biochemistry and control of enzymatic browning. Trends Food Sci. Technol. 6, 195-200.
Masaki, H., 2010. Role of antioxidants in the skin: Anti-aging effects. J. Dermatol. Sci. 58, 85-90.
Mishra, S., Sarkar, U., Taraphder, S., Datta, S., Swain, D., Saikhom, R., 2017. Multivariate statistical data analysis- principal component analysis (PCA). Int. J. Livest. Res. 7(5), 60-78. 
Mohammadhosseini, M., Frezza, C., Venditti, A., Mahdavi, B., 2022. An overview of the genus Aloysia Palau (Verbenaceae): Essential oil composition, ethnobotany and biological activities. Nat. Prod. Res. 36(19), 5091-5107.
Mohammadhosseini, M., Frezza, C., Venditti, A., Sarker, S., 2021. A systematic review on phytochemistry, ethnobotany and biological activities of the genus Bunium L. Chem. Biodivers. 18(11), e2100317.
Newman, D.J., 2008. Natural products as leads to potential drugs: An old process or the new hope for drug discovery? J. Med. Chem. 51, 2589-2599.
Nguyen, M.H., Nguyen, H.X., Nguyen, M.T., Nguyen, N.T., 2012. Phenolic constituents from the heartwood of Artocapusaltilis and their tyrosinase inhibitory activity. Nat. Prod. Commun. 7,185-186.
Nieto, G., 2017. Biological activities of three essential oils of the lamiaceae family. Medicines 4(3), 1-10.
Nouveau, S., Agrawal, D., Kohli, M., Bernerd, F., Misra, N., Nayak, C.S., 2016. Skin hyperpigmentationin Indian population: Insights and best practice. Indian J. Dermatol. 61, 487-95.
Oms-Oliu, G., Hertog, M.L.A., Van de Poel, T.M.B., Ampofo-Asiama, J., Geeraerd, A.H., Nicolaï, B.M., 2011. Metabolic characterization of tomato fruit during preharvest development, ripening, and postharvest shelf-life. Postharvest Biol. Technol. 62, 7-16.
Oyewole, R.O., Oyebamiji, A.K., Semire, B., 2020. Theoretical calculations of molecular descriptors for anticancer activities of 1, 2, 3-triazole-pyrimidine derivatives against gastric cancer cell line (MGC-803): DFT, QSAR and docking approaches. Heliyon 6, e03926.
Pillaiyar, T., Manickam, M., Namasivayam, V., 2017. Skin whitening agents: Medicinal chemistry perspective of tyrosinase inhibitors. J. Enzyme Inhib. Med. Chem. 32 (1), 403-425.
Popović-Djordjević, J., Cengiz, M., Ozer, M.S., Sarikurkcu, C., 2019. Calamintha incana: Essential oil composition and biological activity. Ind. Crops Prod. 128, 162-166.
Prieto, P., Pineda, M., Aguilar, M., 1999. Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: Specific application to the determination of vitamin E. Anal. Biochem. 269, 337-341.
Ragu, S., Faye, G., Iraqui, I., Masurel-Heneman, A., Kolodner, R.D., Huang, M.E., 2007. Oxygen metabolism and reactive oxygenspecies cause chromosomal rearrangements and cell death. Proc. Natl. Acad. Sci. 104, 9747-9752.
Rauf, A., Jehan, N., Senturk M., 2017. Natural Products as a Potential Enzyme Inhibitors From Medicinal Plants. Enzyme Inhibitors and Activators/IntechOpen, Vol. 165, p.177.
Sadasivam, S., Manikam, A., 1992. Biochemical Methods, India. Wiley Eastern Limited.
Sakuma, K., Ogawa, M., Sugibayashi, K., Yamada, K.I., Yamamoto, K., 1999.  Relationship between tyrosinase inhibitory action and oxidation-reduction potential of cosmetic whitening ingredients and phenol derivatives. Arch. Pharm. Res. 22, 335-339.
Sánchez-Ferrer, A., Rodríguez-López, J.N., García-Cánovas, F., García-Carmona, F., 1995. Tyrosinase: A comprehensive reviewof its mechanism. Biochim. Biophys. Acta. 1247, 1-11.
Sasaki, A., Yamano, Y., Sugimoto, S., Otsuka, H., Matsunami, K., Shinzato, T., 2018. Phenolic compounds from the leaves of Breynia officinalis and their tyrosinase and melanogenesis inhibitory activities. J. Nat. Med. 72, 381-389.
Shirota, S., Miyazaki, K., Aiyama, R., Ichioka, M., Yokokura, T., 1994. Tyrosinase inhibitors from crude drugs. Biol. Pharm. Bull. 17, 266-269.
Sumanout, Y., Murakami, Y., Tonda, M., Vajragupta, O., Matsumoto, K., Watanabe, H., 2004. Evaluation of the nitric oxide radical scavenging activity of manganese complexes of curcumin and its derivatives. Biol. Pharm. Bull. 27, 170-173.
Svoboda, K.P., Hampson, J.B., 1999. Bioactivity of essential oils of selected temperate aromatic plants: Antibacterial, antioxidant, anti-inflammatory and other related pharmacological activities. Special Chem. Conf. 16-17.
Tasaka, K., Kamei, C., Nakano, S., 1998. Effects of certain resorcinol derivatives on the tyrosinase activity and the growth of melanoma cells. Methods Find. Exp. Clin. Pharmacol. 20, 99-109.
Vanni, A., Gastaldi, D., Giunata, G., 1990. Kinetic investigation on the double enzyme activity of the mushroom tyrosinase. Anal. Chim. 80, 35-60.