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Current Bioactive Compounds

Editor-in-Chief

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

Research Article

Content Analysis, Cytotoxic, and Anti-metastasis Potential of Bioactive Polysaccharides from Green Alga Codium intricatum Okamura

Author(s): Ross D. Vasquez* and Stephen Lirio

Volume 16, Issue 3, 2020

Page: [320 - 328] Pages: 9

DOI: 10.2174/1573407214666181019124339

Price: $65

Abstract

Background: Codium intricatum, locally known as Pukpuklo, is a seasonal and edible green alga found in Ilocos Norte, Philippines. In this study, the biochemical content, cytotoxic and inhibitory potential against Matrix Metalloproteinase-1 (MMP-1) production of the polysaccharide-protein fractions from C. intricatum is first reported. MMPs are novel targets for therapeutic intervention with the potential to inhibit tumor growth, metastasis and invasion either on their own or in conjunction with cytotoxic treatments.

Methods: Water-soluble Crude Polysaccharide (CP) and its fractions (CFs) from C. intricatum were isolated using hot water and ion-exchange chromatography and analyzed using different analytical techniques. Cytotoxicity against MCF-7 breast cancer cells and Human normal Dermal Fibroblasts (HnDFs) was determined by MTT assay. The MMP-1 inhibitory potential was tested in UVB exposed Human normal Dermal Fibroblast Cells.

Results: CP and CFs afforded carbohydrates (2.07-16.1%), sulfates (1.81%- 9.9%), protein (0.05-2.7%), ash (<77.2%), lipids (<1.0%) and uronic acid (0.15- 4.49%). FT- IR and NMR spectra of CP and CFs exhibited absorption peaks comparable to sulfated galactans. Both CP and CFs significantly inhibited the growth of breast cancer (MCF-7) in a concentration-dependent manner (p<0.05), induced proliferation of HnDFs, inhibited the production of Matrix metalloproteinase-1 (MMP-1) in UV-B induced HnDFs (p<0.05).

Conclusion: Results are highly suggestive that polysaccharide fractions from C. intricatum are bioactive molecules with cytotoxic and anti-metastasis potential.

Keywords: Codium intricatum, cytotoxic effect, matrix metalloproteinase-1 (MMP-1), sulfated polysaccharides, metastasis, fibroblasts.

Graphical Abstract
[1]
Samarakoon, K.; Jeon, Y.J. Bio-functionalities of proteins derived from marine algae: A review. Food Res. Int., 2012, 48(2), 948-960.
[http://dx.doi.org/10.1016/j.foodres.2012.03.013]
[2]
Senthikulmar, K.; Jayachandran, V.; Se-Kwon, K. Marine derived bioactive compounds for breast and prostate cancer treatment: A review. Curr. Bioact. Compd., 2014, 10(1), 62-74.
[http://dx.doi.org/10.2174/1573407210666140327212945]
[3]
Tabarsa, M.; Karnjanapratum, S.; Cho, M.; Kim, J.K.; You, S. Molecular characteristics and biological activities of anionic macromolecules from Codium fragile. Int. J. Biol. Macromol., 2013, 59, 1-12.
[http://dx.doi.org/10.1016/j.ijbiomac.2013.04.022] [PMID: 23597705]
[4]
Karnjanapratum, S.; Tabarsa, M.; Cho, M.; You, S. Characterization and immunomodulatory activities of sulfated polysaccharides from Capsosiphon fulvescens. Int. J. Biol. Macromol., 2012, 51(5), 720-729.
[http://dx.doi.org/10.1016/j.ijbiomac.2012.07.006] [PMID: 22796642]
[5]
Jiao, G.; Yu, G.; Zhang, J.; Ewart, H.S. Chemical structures and bioactivities of sulfated polysaccharides from marine algae. Mar. Drugs, 2011, 9(2), 196-223.
[http://dx.doi.org/10.3390/md9020196] [PMID: 21566795]
[6]
Lee, J.B.; Ohta, Y.; Hayashi, K.; Hayashi, T. Immunostimulating effects of a sulfated galactan from Codium fragile. Carbohydr. Res., 2010, 345(10), 1452-1454.
[http://dx.doi.org/10.1016/j.carres.2010.02.026] [PMID: 20362278]
[7]
Cox, G.; O’Byrne, K.J. Matrix metalloproteinases and cancer. Anticancer Res., 2001, 21(6B), 4207-4219.
[PMID: 11908674]
[8]
Stetler-Stevenson, W.G. The role of matrix metalloproteinases in tumor invasion, metastasis, and angiogenesis. Surg. Oncol. Clin. N.Am., 2001, 10(2), 383-392, x..
[http://dx.doi.org/10.1016/S1055-3207(18)30071-1] [PMID: 11382593]
[9]
Fernández, P.V.; Raffo, M.P.; Alberghina, J.; Ciancia, M. Polysaccharides from the green seaweed Codium decorticatum. Structure and cell wall distribution. Carbohydr. Polym., 2015, 117, 836-844.
[http://dx.doi.org/10.1016/j.carbpol.2014.10.039] [PMID: 25498707]
[10]
Perera, P.C.D. Current potential of seaweeds cultivation in South Asian coastal regions. Agric. Ext. J., 2017, 1(4), 29-34.
[11]
Shao, P.; Chen, M.; Pei, Y.; Sun, P. In intro antioxidant activities of different sulfated polysaccharides from chlorophytan seaweeds Ulva fasciata. Int. J. Biol. Macromol., 2013, 59, 295-300.
[http://dx.doi.org/10.1016/j.ijbiomac.2013.04.048] [PMID: 23643973]
[12]
Dubois, M.; Gilles, K.A.; Hamilton, J.K.; Rebers, P.A.; Smith, F. Colorimetric method for determination of sugars and related substances. Anal. Chem., 1956, 28, 350-356.
[http://dx.doi.org/10.1021/ac60111a017]
[13]
Senthikulmar, D.; Jayanthi, S. Partial characterization and anticancer activities of purified glycoprotein extracted from green seaweed Codiumdecorticatum. J. Funct. Foods, 2016, 25, 323-332.
[http://dx.doi.org/10.1016/j.jff.2016.06.010]
[14]
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(1-2), 248-254.
[http://dx.doi.org/10.1016/0003-2697(76)90527-3] [PMID: 942051]
[15]
You, S.G.; Yang, C.; Lee, H.Y.; Lee, B.Y. Molecular characteristics of partially hydrolyzed fucoidans from sporophyll of Undariapinnatifida and their in vitro anticancer activity. Food Chem., 2010, 119(2), 554-559.
[http://dx.doi.org/10.1016/j.foodchem.2009.06.054]
[16]
Kolmert, A.; Wikström, P.; Hallberg, K.B. A fast and simple turbidimetric method for the determination of sulfate in sulfate-reducing bacterial cultures. J. Microbiol. Methods, 2000, 41(3), 179-184.
[http://dx.doi.org/10.1016/S0167-7012(00)00154-8] [PMID: 10958962]
[17]
Dodgson, K.S.; Price, R.G. A note on the determination of the ester sulphate content of sulphated polysaccharides. Biochem. J., 1962, 84(1), 106-110.
[http://dx.doi.org/10.1042/bj0840106] [PMID: 13886865]
[18]
Melton, L.D.; Smith, G.B. Current Protocols in Food Analytical Chemistry; John Wiley and Sons: New York, 2001.
[19]
Asean Cooperation on Environment (ACE). Asean Marine Water Quality Management Guidelines and Monitoring Manual, 2017.http://environment.asean.org [Accessed May 24, 2018].
[20]
Fernandez, P.V.; Raffoc, M.P.; Albhergina, J.; Ciancia, M. Sulfated β-Dmannan from green seaweed Codiumvermilara. Carbohydr. Polym., 2012, 87(1), 916-919.
[http://dx.doi.org/10.1016/j.carbpol.2011.06.063]
[21]
Renaud, S.M.; Luong-Van, J.T. Seasonal variation in the chemical composition of tropical Australian marine macroalgae. J. Appl. Phycol., 2006, 18, 381-387.
[http://dx.doi.org/10.1007/s10811-006-9034-x]
[22]
Surayot, U.; You, S. Structural effects of sulfated polysaccharides from Codium fragile on NK cell activation and cytotoxicity. Int. J. Biol. Macromol., 2017, 98, 117-124.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.01.108] [PMID: 28130139]
[23]
Ciancia, M.; Quintana, I.; Vizcargüénaga, M.I.; Kasulin, L.; de Dios, A.; Estevez, J.M.; Cerezo, A.S. Polysaccharides from the green seaweeds Codium fragile and C. vermilara with controversial effects on hemostasis. Int. J. Biol. Macromol., 2007, 41(5), 641-649.
[http://dx.doi.org/10.1016/j.ijbiomac.2007.08.007] [PMID: 17920674]
[24]
Dawczynski, C.; Schubert, R.; Jahreis, G. Amino acids, fatty acids, and dietary fiber in edible seaweed products. Food Chem., 2006, 103(3), 891-899.
[http://dx.doi.org/10.1016/j.foodchem.2006.09.041]
[25]
Fan, X.; Bai, L.; Zhu, L.; Yang, L.; Zhang, X. Marine algae-derived bioactive peptides for human nutrition and health. J. Agric. Food Chem., 2014, 62(38), 9211-9222.
[http://dx.doi.org/10.1021/jf502420h] [PMID: 25179496]
[26]
Ngo, D.H.; Kim, S.K. Sulfated polysaccharides as bioactive agents from marine algae. Int. J. Biol. Macromol., 2013, 62, 70-75.
[http://dx.doi.org/10.1016/j.ijbiomac.2013.08.036] [PMID: 23994790]
[27]
Seedevi, P.; Sudharsan, S.; Kumar, S.V.; Srinivasan, A.; Vairamani, S.; Shanmugam, A. Isolation and characterization of sulphated polysaccharides from Codiumtomentosum (J. Stackhouse, 1797) collected from southeast coast of India. Adv. Appl. Sci. Res, 2013, 4, 72-77.
[28]
Liu, K. Characterization of ash in algae and other materials by determination of wet acid indigestible ash and microscopic examination. Algal Res., 2017, 25, 307-321.
[http://dx.doi.org/10.1016/j.algal.2017.04.014]
[29]
Ale, M.T.; Mikkelsen, J.D.; Meyer, A.S. Important determinants for fucoidan bioactivity: a critical review of structure-function relations and extraction methods for fucose-containing sulfated polysaccharides from brown seaweeds. Mar. Drugs, 2011, 9(10), 2106-2130.
[http://dx.doi.org/10.3390/md9102106] [PMID: 22073012]
[30]
Gomez-Ordoñes, E.; Jimenez-Escrig, A.; Ruperez, P. Bioactivity of sulfated polysaccharides from the edible red seaweed Mastocarpusstellatus. Bioact.Carbohydr. Dietary Fibre, 2014, 3(1), 29-40.
[http://dx.doi.org/10.1016/j.bcdf.2014.01.002]
[31]
Seedevi, P.; Moovendhan, M.; Viramani, S.; Shanmugam, A. Bioactive potential and structural chracterization of sulfated polysaccharide from seaweed (Gracilaria corticata). Carbohydr. Polym., 2017, 155, 516-524.
[http://dx.doi.org/10.1016/j.carbpol.2016.09.011] [PMID: 27702543]
[32]
Qi, X.; Mao, W.; Gao, Y.; Chen, Y.; Chen, Y.; Zhao, C.; Li, N.; Wang, C.; Yan, M.; Lin, C.; Shan, J. Chemical characteristic of an anticoagulant-active sulfated polysaccharide from Enteromorpha clathrata. Carbohydr. Polym., 2012, 90(4), 1804-1810.
[http://dx.doi.org/10.1016/j.carbpol.2012.07.077] [PMID: 22944450]
[33]
Kakurakova, M.; Wilson, R.H. Developments in mid-infrared FT-IR spectroscopy of selected carbohydrates. Carbohydr. Polym., 2001, 44(4), 291-303.
[http://dx.doi.org/10.1016/S0144-8617(00)00245-9]
[34]
Souza, B.M.W.S.; Cerqueira, M.A.; Bourbon, A.I.; Pinheiro, A.C.; Martins, T.J.; Teixeira, J.A.; Coimbra, M.A.; Vicente, A.A. Chemical characterization and antioxidant activity of sulfated polysaccharide from the red seaweed Gracilariabirdiae. Food Hydrocoll., 2012, 27(2), 287-292.
[http://dx.doi.org/10.1016/j.foodhyd.2011.10.005]
[35]
Melo, M.R.S.; Freito, J.P.A. Isolation and characterization of soluble sulfated polysaccharide from the red seaweed Gracilaria cornea. Carbohydr. Polym., 2002, 49(4), 491-498.
[http://dx.doi.org/10.1016/S0144-8617(02)00006-1]
[36]
Synytsya, A.; Kim, W.J.; Kim, S.M.; Pohl, R.; Kvasnička, F. Structure and antitumour activity of fucoidan isolated from sporophyll of Korean brown seaweed Undariapinnatifida. Carbohydr. Polym., 2010, 82(1), 41-48.
[http://dx.doi.org/10.1016/j.carbpol.2010.01.052]
[37]
Vishchuk, O.S.; Ermakova, S.P.; Zvyagintseva, T.N. Sulfated polysaccharides from brown seaweeds Saccharina japonica and Undaria pinnatifida: isolation, structural characteristics, and antitumor activity. Carbohydr. Res., 2011, 346(17), 2769-2776.
[http://dx.doi.org/10.1016/j.carres.2011.09.034] [PMID: 22024567]
[38]
Maciel, J.S.; Chaves, L.S. Structural characterization of cold extracted fraction of soluble sulfated polysaccharide from red seaweed Gracilariabirdiae. Carbohydr. Polym., 2008, 71(4), 559-565.
[http://dx.doi.org/10.1016/j.carbpol.2007.06.026]
[39]
Sen, M.; Erboz, E.N. Determination of critical gelation conditions of κ-carrageenan by viscosimetric and FT-IR analyses. Food Res. Int., 2010, 43(5), 1361-1364.
[http://dx.doi.org/10.1016/j.foodres.2010.03.021]
[40]
Shi, Y.; Zhao, L.; Liu, X.; Hu, F.; Cui, F.; Bi, Y.; Ma, Y.; Feng, S. Structural characterization of a sulfated glucan isolated from the aqueous extract of Hedysarumpolybotrys Hand.-Mazz. Carbohydr. Polym., 2012, 87(1), 160-169.
[http://dx.doi.org/10.1016/j.carbpol.2011.07.032]
[41]
Coates, J. Interpretation of Infrared Spectra: A Practical Approach: Encyclopedia of Analytical Chemistry; John Wiley & Sons Ltd.: Chichester, 2000, pp. 10881-10882.
[42]
Pallua, J.D.; Pezzei, C.; Huck-Pezzei, V.A.; Schonbichler, S.; Bittner, K.L.; Bonn, G.K.; Saeed, A.; Majeed, S.; Farooq, A.; Najam-ul-Haq, M.; Abel, G.; Popp, M.; Huck, W.C. Advances of infrared spectroscopic imaging and mapping technologies ofplant material. Curr. Bioact. Compd., 2011, 7(2), 106-117.
[http://dx.doi.org/10.2174/157340711796011179]
[43]
Smyth, E.H.; Cozzolino, D. Applications of infrared spectroscopy for quantitative analysis of volatile and secondary metabolites in plant materials. Curr. Bioact. Compd., 2011, 7(2), 66-74.
[http://dx.doi.org/10.2174/157340711796011160]
[44]
Huck, C. Infrared Spectroscopy of Natural Compounds in Medicinal Plants. Curr. Bioact. Compd., 2011, 7(2), 65.
[http://dx.doi.org/10.2174/157340711796011124]
[45]
Li, N.; Mao, W.; Yan, M.; Liu, X.; Xia, Z.; Wang, S.; Xiao, B.; Chen, C.; Zhang, L.; Cao, S. Structural characterization and anticoagulant activity of a sulfated polysaccharide from the green alga Codium divaricatum. Carbohydr. Polym., 2015, 121, 175-182.
[http://dx.doi.org/10.1016/j.carbpol.2014.12.036] [PMID: 25659687]
[46]
Athukorala, Y.; Kim, K.N.; Jeon, Y.J. Antiproliferative and antioxidant properties of an enzymatic hydrolysate from brown alga, Ecklonia cava. Food Chem. Toxicol., 2006, 44(7), 1065-1074.
[http://dx.doi.org/10.1016/j.fct.2006.01.011] [PMID: 16516367]
[47]
Fukahori, S.; Yano, H.; Akiba, J.; Ogasawara, S.; Momosaki, S.; Sanada, S.; Kuratomi, K.; Ishizaki, Y.; Moriya, F.; Yagi, M.; Kojiro, M. Fucoidan, a major component of brown seaweed, prohibits the growth of human cancer cell lines in vitro. Mol. Med. Rep., 2008, 1(4), 537-542.
[http://dx.doi.org/10.3892/mmr.1.4.537] [PMID: 21479446]
[48]
Fedorov, S.N.; Ermakova, S.P.; Zvyagintseva, T.N.; Stonik, V.A. Anticancer and cancer preventive properties of marine polysaccharides: some results and prospects. Mar. Drugs, 2013, 11(12), 4876-4901.
[http://dx.doi.org/10.3390/md11124876] [PMID: 24317475]
[49]
Kim, A.D.; Lee, Y.; Kang, S.H.; Kim, G.Y.; Kim, H.S.; Hyun, J.W. Cytotoxic effect of clerosterol isolated from Codium fragile on A2058 human melanoma cells. Mar. Drugs, 2013, 11(2), 418-430.
[http://dx.doi.org/10.3390/md11020418] [PMID: 23389088]
[50]
Paradossi, G. Cavalieri, F.;Chiessi, E. A conformational study on the algal polysaccharide ulvan. Macromol., 2002, 35(16), 6404-6411.
[http://dx.doi.org/10.1021/ma020134s]
[51]
Kaeffer, B.; Bénard, C.; Lahaye, M.; Blottière, H.M.; Cherbut, C. Biological properties of ulvan, a new source of green seaweed sulfated polysaccharides, on cultured normal and cancerous colonic epithelial cells. Planta Med., 1999, 65(6), 527-531.
[http://dx.doi.org/10.1055/s-1999-14009] [PMID: 10483372]
[52]
Zong, A.; Cao, H.; Wang, F. Anticancer polysaccharides from natural resources: a review of recent research. Carbohydr. Polym., 2012, 90(4), 1395-1410.
[http://dx.doi.org/10.1016/j.carbpol.2012.07.026] [PMID: 22944395]
[53]
Brenneisen, P.; Wenk, J.; Klotz, L.O.; Wlaschek, M.; Briviba, K.; Krieg, T.; Sies, H.; Scharffetter-Kochanek, K. Central role of Ferrous/Ferric iron in the ultraviolet B irradiation-mediated signaling pathway leading to increased interstitial collagenase (matrix-degrading metalloprotease (MMP)-1) and stromelysin-1 (MMP-3) mRNA levels in cultured human dermal fibroblasts. J. Biol. Chem., 1998, 273(9), 5279-5287.
[http://dx.doi.org/10.1074/jbc.273.9.5279] [PMID: 9478985]
[54]
Moon, H.J.; Lee, S.R.; Shim, S.N.; Jeong, S.H.; Stonik, V.A.; Rasskazov, V.A.; Zvyagintseva, T.; Lee, Y.H. Fucoidan inhibits UVB-induced MMP-1 expression in human skin fibroblasts. Biol. Pharm. Bull., 2008, 31(2), 284-289.
[http://dx.doi.org/10.1248/bpb.31.284] [PMID: 18239288]
[55]
Rasmussen, H.S.; McCann, P.P. Matrix metalloproteinase inhibition as a novel anticancer strategy: a review with special focus on batimastat and marimastat. Pharmacol. Ther., 1997, 75(1), 69-75.
[http://dx.doi.org/10.1016/S0163-7258(97)00023-5] [PMID: 9364582]
[56]
Mohan, V.; Talmi-Frank, D.; Arkadash, V.; Papo, N.; Sagi, I. Matrix metalloproteinase protein inhibitors: highlighting a new beginning for metalloproteinases in medicine. Metalloproteinases Med., 2016, 3, 31-47.
[http://dx.doi.org/10.2147/MNM.S65143]

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