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Current Bioactive Compounds

Editor-in-Chief

ISSN (Print): 1573-4072
ISSN (Online): 1875-6646

Research Article

Bioactive Compounds Isolated from Defatted Microalgal Biomasses of Botryococcus Braunii and Dunaliella Tertiolecta showing a Tyrosinase Inhibitory Activity

Author(s): Da G. Lee, Shaheen A. Kashif, Ah Y. Yoo, Ji W. Choi, Yong I. Park, Andriy Synytsya and Jae K. Park*

Volume 17 , Issue 3 , 2021

Published on: 15 May, 2020

Page: [234 - 245] Pages: 12

DOI: 10.2174/1573407216999200515095507

Price: $65

Abstract

Aims: This study aims to elucidate the structural difference and biochemical properties of bioactive compounds of microalgal biomasses.

Background: The structural difference and biochemical properties of bioactive compounds termed as Water-Soluble Macromolecules (WSMs) are interested in evaluating their biological activities.

Methods: This study was performed to elucidate the structural difference and biochemical properties of bioactive compounds termed as Water-Soluble Macromolecules (WSMs) isolated from defatted microalgal biomasses of Botryococcus braunii and Dunaliella tertiolecta.

Results: The compositional analysis of both WSMs revealed that WSM-Bb is a hetero-macromolecule consisting of various monosaccharides, whereas WSM-Dt was characterized as a homo-- macromolecule that mainly consists of glucose. Interestingly, WSM-Bb showed the significant tyrosinase inhibitory activity with the increase of both the concentration and reaction time. Whereas there was no significant inhibitory activity observed by WSM-Dt.

Conclusion: Inhibitory action of WSM-Bb toward both tyrosinase and tyrosine in either simultaneous or separate reaction may be mainly due to the physical affinity of WSM-Bb. These results emphasize the identification of the primary components of these WSMs and their relevance with the antioxidant function.

Keywords: Microalgae, biomasses, water-soluble macromolecule, antioxidant, tyrosinase, substrate specificity.

Graphical Abstract
[1]
Madkour, F.F.; Abdel-Daim, M.M. Hepatoprotective and antioxidant activity of Dunaliella salina in paracetamol-induced acute toxicity in rats. Indian J. Pharm. Sci., 2013, 75(6), 642-648.
[PMID: 24591738]
[2]
Rao, A.R.; Sarada, R.; Baskaran, V.; Ravishankar, G.A. Antioxidant activity of Botryococcus braunii extract elucidated in vitro models. J. Agric. Food Chem., 2006, 54(13), 4593-4599.
[http://dx.doi.org/10.1021/jf060799j] [PMID: 16787003]
[3]
Yim, J.H.; Son, E.; Pyo, S.; Lee, H.K. Novel sulfated polysaccharide derived from red-tide microalga Gyrodinium impudicumstrain KG03 with immunostimulating activity in vivo. Mar. Biotechnol. (NY), 2005, 7(4), 331-338.
[http://dx.doi.org/10.1007/s10126-004-0404-6] [PMID: 15976942]
[4]
Netanel Liberman, G.; Ochbaum, G.; Malis Arad, S.; Bitton, R. The sulfated polysaccharide from a marine red microalga as a platform for the incorporation of zinc ions. Carbohydr. Polym., 2016, 152, 658-664.
[http://dx.doi.org/10.1016/j.carbpol.2016.07.025] [PMID: 27516316]
[5]
Iqbal, M.J.; Butt, M.S.; Sohail, M.; Suleria, H.A.R. The antioxidant potential of black cumin (Nigella sativa l.) extracts through different extraction methods. Curr. Bioact. Compd., 2019, 15, 623-630.
[http://dx.doi.org/10.2174/1573407214666180821124454]
[6]
Solimine, J.; Garo, E.; Wedler, J.; Rusanov, K.; Fertig, O.; Hamburger, M.; Atanassov, I.; Butterweck, V. Tyrosinase inhibitory constituents from a polyphenol enriched fraction of rose oil distillation wastewater. Fitoterapia, 2016, 108, 13-19.
[http://dx.doi.org/10.1016/j.fitote.2015.11.012] [PMID: 26592852]
[7]
Ding, H.Y.; Lin, H.C.; Chang, T.S. Tyrosinase inhibitors isolated from the roots of Paeonia suffruticosa. J. Cosmet. Sci., 2009, 60(3), 347-352.
[PMID: 19586602]
[8]
Du, Z.Y.; Jiang, Y.F.; Tang, Z.K.; Mo, R.Q.; Xue, G.H.; Lu, Y.J.; Zheng, X.; Dong, C.Z.; Zhang, K. Antioxidation and tyrosinase inhibition of polyphenolic curcumin analogs. Biosci. Biotechnol. Biochem., 2011, 75(12), 2351-2358.
[http://dx.doi.org/10.1271/bbb.110547] [PMID: 22146732]
[9]
Fawole, O.A.; Makunga, N.P.; Opara, U.L. Antibacterial, antioxidant and tyrosinase-inhibition activities of pomegranate fruit peel methanolic extract. BMC Complement. Altern. Med., 2012, 12, 200-211.
[http://dx.doi.org/10.1186/1472-6882-12-200] [PMID: 23110485]
[10]
Fenoll, L.G.; Rodríguez-López, J.N.; Varón, R.; García-Ruiz, P.A.; García-Cánovas, F.; Tudela, J. Kinetic characterisation of the reaction mechanism of mushroom tyrosinase on tyramine/dopamine and L-tyrosine methyl esther/L-dopa methyl esther. Int. J. Biochem. Cell Biol., 2002, 34(12), 1594-1607.
[http://dx.doi.org/10.1016/S1357-2725(02)00076-6] [PMID: 12379281]
[11]
Lee, S.H.; Baek, K.; Lee, J.E.; Kim, B.G. Using tyrosinase as a monophenol monooxygenase: A combined strategy for effective inhibition of melanin formation. Biotechnol. Bioeng., 2016, 113(4), 735-743.
[http://dx.doi.org/10.1002/bit.25855] [PMID: 26461518]
[12]
Zaidi, K.U.; Ali, S.A.; Ali, A.S. Purified mushroom tyrosinase induced melanogenic protein expression in B16F10 melanocytes: A quantitative densitometric analysis. Open Med. Chem. J., 2018, 12, 36-47.
[http://dx.doi.org/10.2174/1874104501812010036] [PMID: 29541257]
[13]
Lee, N.K.; Son, K.H.; Chang, H.W.; Kang, S.S.; Park, H.; Heo, M.Y.; Kim, H.P. Prenylated flavonoids as tyrosinase inhibitors. Arch. Pharm. Res., 2004, 27(11), 1132-1135.
[http://dx.doi.org/10.1007/BF02975118] [PMID: 15595416]
[14]
Solano, F. On the metal cofactor in the tyrosinase family. Int. J. Mol. Sci., 2018, 19(2), 633-650.
[http://dx.doi.org/10.3390/ijms19020633] [PMID: 29473882]
[15]
Sasaki, K.; Yoshizaki, F. Nobiletin as a tyrosinase inhibitor from the peel of citrus fruit. Biol. Pharm. Bull., 2002, 25(6), 806-808.
[http://dx.doi.org/10.1248/bpb.25.806] [PMID: 12081153]
[16]
Chiou, S.Y.; Ha, C.L.; Wu, P.S.; Yeh, C.L.; Su, Y.S.; Li, M.P.; Wu, M.J. Antioxidant, anti-tyrosinase and anti-inflammatory activities of oil production residues from Camellia tenuifloria. Int. J. Mol. Sci., 2015, 16(12), 29522-29541.
[http://dx.doi.org/10.3390/ijms161226184] [PMID: 26690417]
[17]
Nadri, M.H.; Salim, Y.; Basar, N.; Yahya, A.; Zulkifli, R.M. Antioxidant activities and tyrosinase inhibition effects of Phaleria macrocarpa extracts. Afr. J. Tradit. Complement. Altern. Med., 2014, 11(3), 107-111.
[http://dx.doi.org/10.4314/ajtcam.v11i3.16] [PMID: 25371571]
[18]
Sarkhail, P.; Sarkheil, P.; Khalighi-Sigaroodi, F.; Shafiee, A.; Ostad, N. Tyrosinase inhibitor and radical scavenger fractions and isolated compounds from aerial parts of Peucedanum knappii Bornm. Nat. Prod. Res., 2013, 27(10), 896-899.
[http://dx.doi.org/10.1080/14786419.2012.665913] [PMID: 22380985]
[19]
Goo, B.G.; Baek, G.; Choi, D.J.; Park, Y.I.; Synytsya, A.; Bleha, R.; Seong, D.H.; Lee, C.G.; Park, J.K. Characterization of a renewable extracellular polysaccharide from defatted microalgae Dunaliella tertiolecta. Bioresour. Technol., 2013, 129, 343-350.
[http://dx.doi.org/10.1016/j.biortech.2012.11.077] [PMID: 23262010]
[20]
Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 1976, 72, 248-254.
[http://dx.doi.org/10.1016/0003-2697(76)90527-3] [PMID: 942051]
[21]
Du, N.; Tian, W.; Zheng, D.; Zhang, X.; Qin, P. Extraction, purification and elicitor activities of polysaccharides from Chrysanthemum indicum. Int. J. Biol. Macromol., 2016, 82, 347-354.
[http://dx.doi.org/10.1016/j.ijbiomac.2015.10.044] [PMID: 26562553]
[22]
Dubois, M.; Gilles, K.; Hamilton, J.K.; Rebers, P.A.; Smith, F. A colorimetric method for the determination of sugars. Nature, 1951, 168(4265), 167.
[http://dx.doi.org/10.1038/168167a0] [PMID: 14875032]
[23]
Desta, K.T.; Kim, G.S.; Kim, Y.H.; Lee, W.S.; Lee, S.J.; Jin, J.S.; Abd El-Aty, A.M.; Shin, H.C.; Shim, J.H.; Shin, S.C. The polyphenolic profiles and antioxidant effects of Agastache rugosa Kuntze (Banga) flower, leaf, stem and root. Biomed. Chromatogr., 2016, 30(2), 225-231.
[http://dx.doi.org/10.1002/bmc.3539] [PMID: 26094749]
[24]
Navarro, D.; Couturier, M.; da Silva, G.G.; Berrin, J.G.; Rouau, X.; Asther, M.; Bignon, C. Automated assay for screening the enzymatic release of reducing sugars from micronized biomass. Microb. Cell Fact., 2010, 9, 58-68.
[http://dx.doi.org/10.1186/1475-2859-9-58] [PMID: 20637080]
[25]
Lee, D.G.; Choi, D.J.; Park, J.K. Ketoisomeric conversion of glucose derived from microalgal biomasses. Process Biochem., 2015, 50, 941-947.
[http://dx.doi.org/10.1016/j.procbio.2015.03.011]
[26]
Lee, C.G.; Lee, J.; Lee, D.G.; Kim, J.W.; Alnaeeli, M.; Park, Y.I.; Park, J.K. Immunostimulating activity of polyhydric alcohol isolated from Taxus cuspidata. Int. J. Biol. Macromol., 2016, 85, 505-513.
[http://dx.doi.org/10.1016/j.ijbiomac.2016.01.027] [PMID: 26791584]
[27]
Barth, A. Infrared spectroscopy of proteins. Biochim. Biophys. Acta, 2007, 1767(9), 1073-1101.
[http://dx.doi.org/10.1016/j.bbabio.2007.06.004] [PMID: 17692815]
[28]
Fountoulakis, M.; Juranville, J.F.; Manneberg, M. Comparison of the Coomassie brilliant blue, bicinchoninic acid and Lowry quantitation assays, using non-glycosylated and glycosylated proteins. J. Biochem. Biophys. Methods, 1992, 24(3-4), 265-274.
[http://dx.doi.org/10.1016/0165-022X(94)90078-7] [PMID: 1640058]
[29]
Ju, Z.Y.; Deng, D.F.; Dominy, W. A defatted microalgae (Haematococcus pluvialis) meal as a protein ingredient to partially replace fishmeal in diets of Pacific white shrimp (Litopenaeus vannamei, Boone, 1931). Aquacult., 2012, 354-355, 50-55.
[http://dx.doi.org/10.1016/j.aquaculture.2012.04.028]
[30]
Gómez-Ordóñez, E.; Rupérez, P. FTIR-ATR spectroscopy as a tool for macromolecule identification in edible brown and red seaweeds. Food Hydrocoll., 2011, 25, 1514-1520.
[http://dx.doi.org/10.1016/j.foodhyd.2011.02.009]
[31]
Pereira, L.; Gheda, S.F.; Ribeiro-Claro, P.J.A. Analysis by vibrational spectroscopy of seaweed macromolecules with potential use in food, pharmaceutical, and cosmetic industries. Int. J. Carbohydr. Chem., 2013, 2013, 1-7.
[http://dx.doi.org/10.1155/2013/537202]
[32]
Pereira, L.; Amado, A.M.; Critchley, A.T.; van de Velde, F.; Ribeiro-Claro, P.J.A. Identification of selected seaweed macromolecules (phycocolloids) by vibrational spectroscopy (FTIR-ATR and FT-Raman). Food Hydrocoll., 2009, 23, 1903-1909.
[http://dx.doi.org/10.1016/j.foodhyd.2008.11.014]
[33]
Qiu, X.; Amarasekara, A.; Doctor, V. Effect of oversulfation on the chemical and biological properties of fucoidan. Carbohydr. Polym., 2006, 63, 224-228.
[http://dx.doi.org/10.1016/j.carbpol.2005.08.064]
[34]
Sekkal, M.; Legrand, P. A spectroscopic investigation of the carrageenans and agar in the 1500-100 cm−1 spectral range. Spectroch. Acta Part A: Mol. Spectr, 1993, 49, 209-221.
[http://dx.doi.org/10.1016/0584-8539(93)80176-B]
[35]
Yu, P.; Sun, H. Purification of a fucoidan from kelp polysaccharide and its inhibitory kinetics for tyrosinase. Carbohydr. Polym., 2014, 99, 278-283.
[http://dx.doi.org/10.1016/j.carbpol.2013.08.033] [PMID: 24274507]
[36]
Lan, W.C.; Tzeng, C.W.; Lin, C.C.; Yen, F.L.; Ko, H.H. Prenylated flavonoids from Artocarpus altilis: Antioxidant activities and inhibitory effects on melanin production. Phytochemistry, 2013, 89, 78-88.
[http://dx.doi.org/10.1016/j.phytochem.2013.01.011] [PMID: 23465719]
[37]
Li, W.J.; Lin, Y.C.; Wu, P.F.; Wen, Z.H.; Liu, P.L.; Chen, C.Y.; Wang, H.M. Biofunctional constituents from Liriodendron tulipifera with antioxidants and anti-melanogenic properties. Int. J. Mol. Sci., 2013, 14(1), 1698-1712.
[http://dx.doi.org/10.3390/ijms14011698] [PMID: 23322020]
[38]
Chen, Y.H.; Huang, L.; Wen, Z.H.; Zhang, C.; Liang, C.H.; Lai, S.T.; Luo, L.Z.; Wang, Y.Y.; Wang, G.H. Skin whitening capability of shikimic acid pathway compound. Eur. Rev. Med. Pharmacol. Sci., 2016, 20(6), 1214-1220.
[PMID: 27049279]
[39]
Alam, N.; Yoon, K.N.; Lee, K.R.; Kim, H.Y.; Shin, P.G.; Cheong, J.C.; Yoo, Y.B.; Shim, M.J.; Lee, M.W.; Lee, T.S. Assessment of antioxidant and phenolic compound concentrations as well as xanthine oxidase and tyrosinase inhibitory properties of different extracts of Pleurotus citrinopileatus fruiting bodies. Mycobiology, 2011, 39(1), 12-19.
[http://dx.doi.org/10.4489/MYCO.2011.39.1.012] [PMID: 22783067]
[40]
Mitani, K.; Takano, F.; Kawabata, T.; Allam, A.E.; Ota, M.; Takahashi, T.; Yahagi, N.; Sakurada, C.; Fushiya, S.; Ohta, T. Suppression of melanin synthesis by the phenolic constituents of sappanwood (Caesalpinia sappan). Planta Med., 2013, 79(1), 37-44.
[PMID: 23154842]
[41]
Takahashi, M.; Takara, K.; Toyozato, T.; Wada, K. A novel bioactive chalcone of Morus australis inhibits tyrosinase activity and melanin biosynthesis in B16 melanoma cells. J. Oleo Sci., 2012, 61(10), 585-592.
[http://dx.doi.org/10.5650/jos.61.585] [PMID: 23018855]
[42]
Khan, S.; Khan, M.T.H.; Kardar, M.N. Tyrosinase Inhibitors from the fruits of Madhuca latifolia. Curr. Bioact. Compd., 2014, 10, 31-36.
[http://dx.doi.org/10.2174/1573407210666140311234806]
[43]
Tanabe, Y.; Okazaki, Y.; Yoshida, M.; Matsuura, H.; Kai, A.; Shiratori, T.; Ishida, K.; Nakano, S.; Watanabe, M.M. A novel alphaproteobacterial ectosymbiont promotes the growth of the hydrocarbon-rich green alga Botryococcus braunii. Sci. Rep., 2015, 5, 10467-10478.
[http://dx.doi.org/10.1038/srep10467] [PMID: 26130609]
[44]
Weiss, T.L.; Roth, R.; Goodson, C.; Vitha, S.; Black, I.; Azadi, P.; Rusch, J.; Holzenburg, A.; Devarenne, T.P.; Goodenough, U. Colony organization in the green alga Botryococcus braunii (Race B) is specified by a complex extracellular matrix. Eukaryot. Cell, 2012, 11(12), 1424-1440.
[http://dx.doi.org/10.1128/EC.00184-12] [PMID: 22941913]
[45]
Xiao, R.; Zheng, Y. Overview of microalgal Extracellular Polymeric Substances (EPS) and their applications. Biotechnol. Adv., 2016, 34(7), 1225-1244.
[http://dx.doi.org/10.1016/j.biotechadv.2016.08.004] [PMID: 27576096]

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