Biochemical profiling and anticancer properties of brown seaweed Dictyota dichotoma (Hudson.) J.V.Lamouroux
Subject Areas : Phytochemistry: Isolation, Purification, CharacterizationVelankanni Arputhaswamy 1 , Vasanthkumar Rajkumar 2 , Nancy Mary Thomas 3 , Vinoth Sathasivam 4 , Arun Muthukrishnan 5 , Gurusaravanan Packiaraj 6 *
1 - Plant Biotechnology Laboratory, Department of Botany, Bharathiar University, Coimbatore-641 046, Tamil Nadu, India
2 - Plant Biotechnology Laboratory, Department of Botany, Bharathiar University, Coimbatore-641 046, Tamil Nadu, India
3 - Plant Biotechnology Laboratory, Department of Botany, Bharathiar University, Coimbatore-641 046, Tamil Nadu, India
4 - Department of Biotechnology, Sona College of Arts and Science, Salem-636 005, Tamil Nadu, India
5 - Department of Biotechnology, Bharathiar University, Coimbatore-641 046, Tamil Nadu, India
6 - Plant Biotechnology Laboratory, Department of Botany, Bharathiar University, Coimbatore-641 046, Tamil Nadu, India
Keywords: Anticancer, Antioxidant, Biochemical profiling, Dictyota dichotoma (Hudson.) J.V.Lamouroux, MCF-7 cancer cell,
Abstract :
In the present study, we have extracted the secondary metabolites from Dictyota dichotoma and evaluated their anticancer properties against Michigan Cancer Foundation-7 (MCF-7) breast cancer cell lines. Different solvent extracts were used to isolate the bioactive molecules form D. dichotoma. Among them, methanol extract showed the highest total phenol content (TPC: 306.31 ± 1.7 GAE mg/g extract), total tannin content (TTC: 291.90 ± 1.2 RE mg/g extract) and total flavonoid content (TFC: 92.89 ± 0.6 GAE mg/g extract). The antioxidant ABTS assay of methanol extract inhibited 74.51 ± 0.10% of free radicals and phosphomolybdenum assay showed 62.36 ± 0.04 mg/g AAE/g extract. Furthermore, bioactive compounds were characterised by gas chromatography-mass spectroscopy (GC-MS), highly performance liquid chromatography (HPLC) and Fourier transmission infrared spectroscopy (FT-IR). The GC-MS results revealed 29 bioactive compounds that are highly potential biological activities. The extracted compound was quantified and confirmed by HPLC and FT-IR. The D. dichotoma methanol extract effectively induced the apoptosis in MCF-7 breast cancer cells and recorded IC50 value of 44.35 ± 8.62 µg/mL.
Adeosun, C.B., Olaseinde, S., Opeifa, A., Atolani, O., 2013. Essential oil from the stem bark of Cordia sebestena scavenges free radicals. J. Acute Med. 3(4), 138-141.
Ahmed, A., Akbar, S., Shah, W.A., 2017. Chemical composition and pharmacological potential of aromatic water from Salix caprea inflorescence. Chin. J. Integr. Med. 1-5, doi: 10.1007/s11655-017-2781-5.
Akbari, A., Bigham, A., Rahimkhoei, V., Sharifi, S., Jabbari, E., 2022. Antiviral polymers: A review. Polymers 14(9), 1634.
Akhir, F.N.M., Nazaruddin, F.H.M., Hara, H., Ahmad, I., 2022. Role of Algae in Cancer. Handbook of Research on Algae as a Sustainable Solution for Food, Energy, and the Environment, pp. 562-584.
Al-Rubaye, A.F., Kaizal, A.F., Hameed, I.H., 2017. Phytochemical screening of methanolic leaves extract of Malva sylvestris. Int. J. Pharmacogn. Phytochem. Res. 9(4), 537-552.
Aldarhami, A., Bazaid, A.S., Alhamed, A.S., Alghaith, A.F., Ahamad, S.R., Alassmrry, Y.A., Alharazi, T., Snoussi, M., Qanash, H., Alamri, A., 2023. Antimicrobial potential of Pithecellobium dulce seed extract against pathogenic bacteria: In silico and in vitro evaluation. Biomed Res. Int. 2023 , 2848198.
Ameen, F., AlNadhari, S., Al-Homaidan, A.A., 2021. Marine microorganisms as an untapped source of bioactive compounds. Saudi J. Biol. Sci. 28(1), 224-231.
Ammar, M.B., Ayachi, F.L., Ksantini, R., Mahjoubi, H., 2022. Data warehouse for machine learning: Application to breast cancer diagnosis. Procedia Comput. Sci. 196, 692-698.
Amos-Tautua, B.M., Alayande, K.A., Ajileye, O., Fadare, O.A., Songca, A.O.S.P., 2020. Effect of the leaf extracts of Funtumia africana (Benth.) Stapf. against selected pathogens. J. Med. Plants Stud. 8(4), 125-129.
Azmir, J., Zaidul, I.S.M., Rahman, M.M., Sharif, K., Mohamed, A., Sahena, F., Jahurul, M., Ghafoor, K., Norulaini, N., Omar, A., 2013. Techniques for extraction of bioactive compounds from plant materials: A review. J. Food Eng. 117(4), 426-436.
Blois, M.S., 1958. Antioxidant determinations by the use of a stable free radical. Nature 181(4617), 1199-1200.
Bogaert, K.A., Delva, S., De Clerck, O., 2020. Concise review of the genus Dictyota JV Lamouroux. J. Appl. Phycol. 32, 1521-1543.
Budhiyanti, S.A., Raharjo, S., Marseno, D.W., Lelana, I.Y., 2012. Antioxidant activity of brown algae Sargassum species extracts from the coastline of Java Island. Am. J. Agric. Biol. Sci. 7(3), 337-346.
Chakraborty, K., Joseph, D., Praveen, N.K., 2015. Antioxidant activities and phenolic contents of three red seaweeds (Division: Rhodophyta) harvested from the Gulf of Mannar of Peninsular India. J. Food Sci. Technol. 52, 1924-1935.
Chaudhary, Z., Subramaniam, S., Khan, G.M., Abeer, M.M., Qu, Z., Janjua, T., Kumeria, T., Batra, J., Popat, A., 2019. Encapsulation and controlled release of resveratrol within functionalized mesoporous silica nanoparticles for prostate cancer therapy. Front. Bioeng. Biotechnol. 7, 225.
Dang, T.T., Bowyer, M.C., Van Altena, I.A., Scarlett, C.J., 2018. Comparison of chemical profile and antioxidant properties of the brown algae. Int. J. Food Sci. Technol. 53(1), 174-181.
Deyab, M.A., Ward, F., 2016. Ecological and biochemical analyses of the brown algae Turbinaria ornata (Turner) J. Agardh from Red Sea coast, Egypt. J. Coast. Life Med. 4(3), 187-192.
Diem, M., Romeo, M., Boydston-White, S., Miljković, M., Matthäus, C., 2004. A decade of vibrational micro-spectroscopy of human cells and tissue (1994-2004). Analyst 129(10), 880-885.
El Gamal, A.A., 2010. Biological importance of marine algae. Saudi Pharm. J. 18(1), 1-25.
Ferdous, U.T., Yusof, Z.N.B., 2021. Medicinal prospects of antioxidants from algal sources in cancer therapy. Front. Pharmacol. 12, 593116.
Ferlay, J., Colombet, M., Soerjomataram, I., Parkin, D.M., Piñeros, M., Znaor, A., Bray, F., 2021. Cancer statistics for the year 2020: An overview. Int. J. Cancer 149(4), 778-789.
Fidyt, K., Fiedorowicz, A., Strządała, L., Szumny, A., 2016. β‐Caryophyllene and β‐caryophyllene oxide—natural compounds of anticancer and analgesic properties. Cancer Med. 5(10), 3007-3017.
Freile‐Pelegrín, Y., Robledo, D., 2013. Bioactive Phenolic Compounds from Algae. Bioactive Compounds from Marine Foods: Plant and Animal Sources. Wiley Publication. pp. 113-129.
Ganesan, A.R., Shanmugam, M., 2020. Isolation of phycoerythrin from Kappaphycus alvarezii: A potential natural colourant in ice cream. J. Appl. Psychol. 32, 4221-4233.
Giriwono, P.E., Iskandriati, D., Tan, C.P., Andarwulan, N., 2019. Sargassum seaweed as a source of anti-inflammatory substances and the potential insight of the tropical species: A review. Mar. Drugs 17(10), 590.
Habeebullah, S.F.K., Alagarsamy, S., 2023. Bioactive Secondary Metabolites From Marine Macroalgae, Algal Metabolites. Apple Academic Press, pp. 339-400.
Hadi, M.Y., Mohammed, G.J., Hameed, I.H., 2016. Analysis of bioactive chemical compounds of Nigella sativa using gas chromatography-mass spectrometry. J. Pharmacognosy Phytother. 8(2), 8-24.
Hakim, M., Patel, I., 2023. Phytochemical evaluation, FT-IR and RP-HPLC analysis of marine brown algae collected from the coastal area of Okha in Gujarat. Egypt. J. Agric. Res. 101(1), 54-60.
Harborne, P.D., 1999. Handbook of Bioactive Compounds from Plants 2nd (Edn.) Taylor and Francis. London.
Hasan, M., Imran, M.A.S., Bhuiyan, F.R., Ahmed, S.R., Shanzana, P., Moli, M.A., Foysal, S.H., Dabi, S.B., 2019. Phytochemical constituency profiling and antimicrobial activity screening of seaweeds extracts collected from the Bay of Bengal sea coasts. BioRxiv 680348.
Hosseini, A., Mousavi, S.H., Ghanbari, A., Shandiz, F.H., Raziee, H.R., Rad, M.P., Mousavi, S.H., 2015. Effect of saffron on liver metastases in patients suffering from cancers with liver metastases: A randomized, double blind, placebo-controlled clinical trial. Avicenna J. Phytomed. 5(5), 434.
Huang, X., Li, S., Ding, R., Li, Y., Li, C., Gu, R., 2023. Antitumor effects of polysaccharides from medicinal lower plants: A review. Int. J. Biol. Macromol. 252, 126313.
Jayapala, N., Perumal, M.K., Baskaran, R., Vallikannan, B., 2022. Pharmacological Importance of Bioactive Molecules of Seaweeds, Sustainable Global Resources of Seaweeds Vol. 2: Food, Pharmaceutical and Health Applications. Springer, pp. 597-613.
Jayawardena, T.U., Kim, H.-S., Sanjeewa, K.A., Kim, S.-Y., Rho, J.-R., Jee, Y., Ahn, G., Jeon, Y.-J., 2019. Sargassum horneri and isolated 6-hydroxy-4, 4,7a-trimethyl-5,6,7, 7a-tetrahydrobenzofuran-2 (4H)-one (HTT); LPS-induced inflammation attenuation via suppressing NF-κB, MAPK and oxidative stress through Nrf2/HO-1 pathways in RAW 264.7 macrophages. Algal Res. 40, 101513.
Jimenez-Lopez, C., Pereira, A., Lourenço-Lopes, C., García-Oliveira, P., Cassani, L., Fraga-Corral, M., Prieto, M., Simal-Gandara, J., 2021. Main bioactive phenolic compounds in marine algae and their mechanisms of action supporting potential health benefits. Food Chem. 341, 128262.
Keskinkaya, H.B., Deveci, E., Altinok, B.Y., Gümüş, N.E., Aslan, E.S.O., Akköz, C., Karakurt, S., 2023. HPLC-UV analysis of phenolic compounds and biological activities of Padina pavonica and Zanardinia typus marine macroalgae species. Turk. J. Bot. 47(3), 231-243.
Khan, M.Z., Azad, A.K., Jan, S., Safdar, M., Bibi, S., Majid, A.M.S.A., Albadrani, G.M., Nouh, N.A.T., Abdulhakim, J.A., Abdel-Daim, M.M., 2023. An experimental and computational analysis of plant compounds from whole Urtica dioica L. plant’s essential oil for antioxidant and antibacterial activities. Metabolites 13(4), 502.
Kim, S.-K., Wijesekara, I., 2010. Development and biological activities of marine-derived bioactive peptides: A review. J. Funct. Foods 2(1), 1-9.
Kumar, Y., Singhal, S., Tarafdar, A., Pharande, A., Ganesan, M., Badgujar, P.C., 2020. Ultrasound assisted extraction of selected edible macroalgae: Effect on antioxidant activity and quantitative assessment of polyphenols by liquid chromatography with tandem mass spectrometry (LC-MS/MS). Algal Res. 52, 102114.
Madhavan, M., 2015. Phytochemical constituents of leaves of Spatholobus parviflorus a rare threatened climber of South India. Int. J. Pharmacogn. Phytochem. Res. 7(5), 991-994.
Mahdavi, B., Mohammadhosseini, M., 2022. Antioxidant, antimicrobial and anti-prostate cancer activity of the extracts from different parts of Etlingera velutina (Ridl.) R. M. Sm (Zingiberaceae). Trends Phytochem. Res. 6(4), 353-362.
Mahendran, S., Sankaralingam, S., Sethupathi, S.M., Kathiresan, D., Muthumani, M., Kousalya, L., Palpperumal, S., Harinathan, B., 2022. Evaluation of antioxidant and cytotoxicity activities of polyphenol extracted from brown seaweed Sargassum tenerrimum biomass. Biomass Convers. Biorefin. 14(2), 2063-2069.
Makkar, H.P., Makkar, H.P., 2003. Measurement of Total Phenolics and Tannins Using Folin-Ciocalteu Method. Quantification of Tannins in Tree and Shrub Foliage: A Laboratory Manual, pp. 49-51.
Mitić, Z.S., Jovanović, B., Jovanović, S.Č., Stojanović-Radić, Z.Z., Mihajilov-Krstev, T., Jovanović, N.M., Nikolić, B.M., Marin, P.D., Zlatković, B.K., Stojanović, G.S., 2019. Essential oils of Pinus halepensis and P. heldreichii: Chemical composition, antimicrobial and insect larvicidal activity. Ind. Crops Prod. 140, 111702.
Mosmann, T., 1983. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods 65(1-2), 55-63.
Nakaziba, R., Amanya, S.B., Sesaazi, C.D., Byarugaba, F., Ogwal-Okeng, J., Alele, P.E., 2022. Antimicrobial bioactivity and GC-MS analysis of different extracts of Corchorus olitorius L leaves. Sci. World J. 2022.
Namvar, F., Baharara, J., Mahdi, A., 2014. Antioxidant and anticancer activities of selected Persian Gulf algae. Indian J. Clin. Biochem. 29, 13-20.
Naveen, J., Baskaran, R., Baskaran, V., 2021. Profiling of bioactives and in vitro evaluation of antioxidant and antidiabetic property of polyphenols of marine algae Padina tetrastromatica. Algal Res. 55, 102250.
Olejniczak, T., 2010. Microbial hydroxylation of non-activated carbon atoms in racemic 2-dodeceno-1-yl-succinic anhydride by Mortierella isabellina 212. World J. Microbiol. Biotechnol. 26, 2053-2060.
Pádua, D., Rocha, E., Gargiulo, D., Ramos, A., 2015. Bioactive compounds from brown seaweeds: Phloroglucinol, fucoxanthin and fucoidan as promising therapeutic agents against breast cancer. Phytochem. Lett. 14, 91-98.
Pan, Z., Wang, S.-K., Cheng, X.-L., Tian, X.-W., Wang, J., 2016. Caryophyllene oxide exhibits anti-cancer effects in MG-63 human osteosarcoma cells via the inhibition of cell migration, generation of reactive oxygen species and induction of apoptosis. Bangladesh J. Pharmacol. 11(4), 817-823.
Paul, J.P.J., 2018. Phytochemical analysis of methanolic extract of Caulerpa scalpelliformis (r. Br.) Web. V. Bosse collected from hare island, thoothukudi, tamil nadu, India. Indo Am. J. Pharm. 5(3), 1905-1908.
Popwo Tameye, S.C., Ndom, J.C., Nguemfo, E.L., Wansi, J.D., Vardamides, J.C., Azebaze, A.G.B., 2020. Ficusanol, a new cinnamic acid derivative and other constituents from the roots of Ficus exasperata Vahl.(Moraceae) with antioxidant and cytotoxic activities. Trends Phytochem. Res. 4(1), 3-8.
Prasher, I.B., Manju, 2019. Screening of Peniophora nuda (a white rot fungus) for the presence of commercially important bioactive metabolites. Vegetos 32(3), 307-315.
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(2), 337-341.
Raj, E.D.S., 2016. UV-VIS and HPLC studies on Amphiroa anceps (Lamarck) Decaisne. Arab. J. Chem. 9, S907-S913.
Raja, K., Vignesh, A., Lavanya, P., Ravi, M., Selvakumar, S., Vasanth, K., 2023. Organosulfur compound identified from Striga angustifolia (D. Don) CJ Saldanha inhibits lung cancer growth and induces apoptosis via p53/mTOR signaling pathway. Appl. Biochem. Biotechnol. 195(12), 7277-7297.
Raman, B.V., Samuel, L., Saradhi, M.P., Rao, B.N., Krishna, N., Sudhakar, M., Radhakrishnan, T., 2012. Antibacterial, antioxidant activity and GC-MS analysis of Eupatorium odoratum. Asian J. Pharm. Clin. Res. 5(2), 99-106.
Rattaya, S., Benjakul, S., Prodpran, T., 2015. Extraction, antioxidative, and antimicrobial activities of brown seaweed extracts, Turbinaria ornata and Sargassum polycystum, grown in Thailand. Int. Aquat. Res. 7, 1-16.
Rebours, C., Marinho-Soriano, E., Zertuche-González, J.A., Hayashi, L., Vásquez, J.A., Kradolfer, P., Soriano, G., Ugarte, R., Abreu, M.H., Bay-Larsen, I., 2014. Seaweeds: An opportunity for wealth and sustainable livelihood for coastal communities. J. Appl. Phycol. 26, 1939-1951.
Rengasamy, K.R., Mahomoodally, M.F., Aumeeruddy, M.Z., Zengin, G., Xiao, J., Kim, D.H., 2020. Bioactive compounds in seaweeds: An overview of their biological properties and safety. Food Chem. Toxicol. 135, 111013.
Rocha, D.H., Seca, A.M., Pinto, D.C., 2018. Seaweed secondary metabolites in vitro and in vivo anticancer activity. Mar. Drugs 16(11), 410.
Sakthivel, R., Devi, K.P., 2019. Antioxidant, anti-inflammatory and anticancer potential of natural bioactive compounds from seaweeds. Stud. Nat. Prod. Chem. 63, 113-160.
Sánchez-Mendoza, M.E., Cruz-Antonio, L., GuadalupeCupido-Sánchez, M., GarcíaCastillo, G., Arrieta, J., 2014. Gastroprotective activity of caryophyllene oxide: The role of nitric oxide, prostaglandins and sulfhydryls. J. Appl. Pharm. Sci. 4(9), 001-005.
Shaaban, M.T., Ghaly, M.F., Fahmi, S.M., 2021. Antibacterial activities of hexadecanoic acid methyl ester and green‐synthesized silver nanoparticles against multidrug‐resistant bacteria. J. Basic Microbiol. 61(6), 557-568.
Shanab, S.M., Shalaby, E.A., 2012. The first record of biological activities of the Egyptian red algal species Compsopogon helwanii. Int. J. Biosci. Biochem. Bioinformatics 2(4), 291.
Sivakumar, S., Vignesh, A., 2014. In vitro activity of seaweed extracts collected from Gulf of Mannar coast islands Tamilnadu on clinical isolates. WJFMS 6(6), 504-508.
Soliman, Y.A., Ibrahim, A.M., Tadros, H.R., Abou-Taleb, A.E., Moustafa, A.H., Hamed, M.A., 2016. Antifouling and antibacterial activities of marine bioactive compounds extracted from some red sea cucumber. Contemp. Appl. Sci. 3, 83-103.
Thouri, A., Chahdoura, H., El Arem, A., Omri Hichri, A., Ben Hassin, R., Achour, L., 2017. Effect of solvents extraction on phytochemical components and biological activities of Tunisian date seeds (var. Korkobbi and Arechti). BMC Complement. Altern. Med. 17(1), 1-10.
Tyagi, T., Agarwal, M., 2017. GC-MS analysis of invasive aquatic weed, Pistia stratiotes L. and Eichhornia crassipes (Mart.) Solms. Int. J. Curr. Pharm. Res. 9(3), 111.
Venkatesan, M., Sekhar, S.C., Sathyamurthy, R., Athikesavan, M.M., 2023. Experimental investigation on seaweed (Sargassum wightii) derived using methanolic extracts. Alex. Eng. J. 68, 453-460.
Vignesh, A., Amal, T.C., Selvakumar, S., Vasanth, K., 2023. Unraveling the role of medicinal plants and Gut microbiota in colon cancer: Towards microbiota-based strategies for prevention and treatment. Health Sci. Rev. 100115.
Vignesh, A., Sivalingam, R., Selvakumar, S., Vasanth, K., 2022. A review on ethnomedicinal and phytopharmacological potential of traditionally wild and endemic plant Berberis tinctoria Lesch. Thai J. Pharm. Sci. 46(2), 137-148.
Xin, Z., Zhang, M., Cui, H., Ding, X., Zhang, T., Wu, L., Cui, H., Xue, Q., Chen, C., Gao, J., 2023. Algae: A robust living material against cancer. Int. J. Nanomedicine 5243-5264.
Yamuna Devi, M., Wesely, E., Johnson, M., 2012. Chromatographic studies on the tannins of Aerva lanata (L.) Juss. Ex Schultes. IOSR J. Pharm. 2(1), 41-51.
Zhang, J., Wen, C., Zhang, H., Duan, Y., Ma, H., 2020. Recent advances in the extraction of bioactive compounds with subcritical water: A review. Trends Food Sci. 95, 183-195.