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Bioprospecting of brown seaweed (Ochrophyta) from the Yucatan Peninsula: cytotoxic, antiproliferative, and antiprotozoal activities

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Abstract

In the Yucatan Peninsula coast, a large diversity of seaweed species are found, and recent studies have reported the presence of metabolites with pharmaceutical importance. In this study, a biological screening of brown seaweed extracts from Dictyota ciliolata, Padina sanctae-crucis, Sargassum fluitans, and Turbinaria tricostata was carried out. Their cytotoxicity and antiproliferative activities were evaluated by the sulforhodamine B assay on human embryonic kidney (HEK 293), human breast cancer (MCF-7), human prostate cancer (LNCaP), and human hepatic cancer (Hep-G2) cell lines. Seaweed extracts were also tested for their anti-trichomonal (Trichomonas vaginalis) and anti-giardicidal (Giardia lamblia) properties. Fucan fractions were extracted using successive maceration with ethanol/water and freeze-dried. Organics extracts were obtained from ethanol residue from liquid–liquid fractionation. A total of four ethanol extracts, four fucan-rich fractions, four ethanolic extracts, and 12 organic fractions were obtained. Only the ethanolic extracts from Turbinaria tricostata and D. ciliolata were active against LNCaP (CC50 of 24.4 and 29.3 μg mL−1, respectively). Interestingly, the activity found in the extracts from D. ciliolata and Turbinaria tricostata was maintained when both extracts were subjected to a liquid–liquid fractionation with hexane on the LNCaP cell line (CC50 of 24.4 and 25.2 μg mL−1, respectively). The antiproliferative assays showed that both dichloromethane and ethanolic fractions from P. sanctae-crucis were active against MCF-7, with IC50 of 26.1 and 29.8 μg mL−1, respectively. These species have been selected for further bio-guided fractionation and isolation of active compounds.

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References

  • Ale MT, Maruyama H, Tamauchi H, Mikkelsen JD, Meyer AS (2011) Fucose-containing sulfated polysaccharides from brown seaweeds inhibit proliferation of melanoma cells and induce apoptosis by activation of caspase-3 in vitro. Mar Drugs 9:2605–2621

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Asari F, Kusumi T, Kakisawa H (1989) Turbinaric acid, a cytotoxic secosqualene carboxylic acid from the brown alga Turbinaria ornata. J Nat Prod 52:1167–1169

    Article  PubMed  CAS  Google Scholar 

  • Awad NE, Selim MA, Metawe HM, Matloub AA (2008) Cytotoxic xenicane diterpenes from the brown alga Padina pavonia (L.) Gaill. Phytother Res 22:1610–1613

    Article  PubMed  CAS  Google Scholar 

  • Ayyad SE, Makki MS, Al-Kayal NS, Basaif SA, El-Foty KO, Asiri AM, Alarif WM, Badria FA (2011) Cytotoxic and protective DNA damage of three new diterpenoids from the brown alga Dictoyota dichotoma. Eur J Med Chem 46:175–182

    Article  PubMed  CAS  Google Scholar 

  • Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR (2013) Marine natural products. Nat Prod Rep 30:237–323

    Article  PubMed  CAS  Google Scholar 

  • Cantillo-Ciau Z, Moo-Puc R, Quijano L, Freile-Pelegrín Y (2010) The tropical brown alga Lobophora variegata: a source of antiprotozoal compounds. Mar Drugs 16:1292–1304

    Article  CAS  Google Scholar 

  • Cedillo-Rivera R, Chávez B, González-Robles A, Tapia A, Yépez-Mulia L (2002) In vitro effect of nitazoxanide against Entamoeba histolytica, Giardia intestinalis and Trichomonas vaginalis trophozoites. J Eukaryot Microbiol 49:201–208

    Article  PubMed  CAS  Google Scholar 

  • Cronin G, Lindquist NL, Hay ME, Fenical W (1995) Effects of storage and extraction procedures on yields of lipophilic metabolites from the brown seaweeds Dictyota ciliolata and D. menstrualis. Mar Ecol Prog Ser 119:265–273

    Article  Google Scholar 

  • Dantas-Santos N, Almeida-Lima J, Vidal AA, Gomes DL, Oliveira RM, Santos Pedrosa S, Pereira P, Gama FM, Oliveira Rocha HA (2012) Antiproliferative activity of fucan nanogel. Mar Drugs 10:2002–2022

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dore CM, Faustino Alves MG, Will LS, Costa TG, Sabry DA, de Souza Rêgo LA, Accardo CM, Rocha HA, Filgueira LG, Leite EL (2013) A sulfated polysaccharide, fucans, isolated from brown algae Sargassum vulgare with anticoagulant, antithrombotic, antioxidant and anti-inflammatory effects. Carbohydr Polym 91:467–475

    Article  PubMed  CAS  Google Scholar 

  • Faulkner DJ (2002) Marine natural products. Nat Prod Rep 19:1–49

    PubMed  CAS  Google Scholar 

  • Foley SA, Mulloy B, Tuohy MG (2011) An unfractionated fucoidan from Ascophyllum nodosum: extraction, characterization, and apoptotic effects in vitro. J Nat Prod 74:851–1861

    Article  CAS  Google Scholar 

  • Freile-Pelegrin Y, Robledo D, Chan-Bacab MJ, Ortega-Morales BO (2008) Antileishmanial properties of tropical marine algae extracts. Fitoterapia 79:374–377

    Article  PubMed  CAS  Google Scholar 

  • Gedara SR, Abdel-Halim OB, el-Sharkawy SH, Salama OM, Shier TW, Halim AF (2003) Cytotoxic hydroazulene diterpenes from the brown alga Dictyota dichotoma. Z Naturforsch C 58:17–22

    PubMed  CAS  Google Scholar 

  • Hu GP, Yuan J, Sun L, She ZG, Wu JH, Lan XJ, Zhu X, Lin YC, Chen SP (2011) Statistical research on marine natural products based on data obtained between 1985 and 2008. Mar Drugs 9:514–525

    Article  PubMed Central  PubMed  Google Scholar 

  • Ioannou E, Quesada A, Rahman MM, Gibbons S, Vagias C, Roussis V (2011) Dolabellanes with antibacterial activity from the brown alga Dilophus spiralis. J Nat Prod 25:213–222

    Article  CAS  Google Scholar 

  • Jiao G, Yu G, Zhang J, Ewart HS (2011) Chemical structures and bioactivities of sulfated polysaccharides from marine algae. Mar Drugs 9:196–223

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jongaramruong J, Kongkam N (2007) Novel diterpenes with cytotoxic, anti-malarial and anti-tuberculosis activities from a brown alga Dictyota sp. J Asian Nat Prod Res 9:743–751

    Article  PubMed  CAS  Google Scholar 

  • Jung KA, Lim SR, Kim Y, Park JM (2013) Potentials of macroalgae as feedstocks for biorefinery. Bioresour Technol 135:182–190

    Article  PubMed  CAS  Google Scholar 

  • Kim SM, Kang K, Jeon JS, Jho EH, Kim CY, Nho CW, Um BH (2011) Isolation of phlorotannins from Eisenia bicyclis and their hepatoprotective effect against oxidative stress induced by tert-butyl hyperoxide. Appl Biochem Biotechnol 165:1296–1307

    Article  PubMed  CAS  Google Scholar 

  • Ktari L, Guyot M (1999) A cytotoxic oxysterol from the marine alga Padina pavonica (L.) Thivy. J Appl Phycol 11:511–513

    Article  CAS  Google Scholar 

  • Lee JI, Seo Y (2011) Chromanols from Sargassum siliquastrum and their antioxidant activity in HT 1080 cells. Chem Pharm Bull 59:757–761

    Article  PubMed  CAS  Google Scholar 

  • León-Deniz LV, Dumonteil E, Moo-Puc R, Freile-Pelegrin Y (2009) Antitrypanosomal in vitro activity of tropical marine algae extracts. Pharm Biol 47:864–871

    Article  Google Scholar 

  • Manzoa E, Ciavattaa ML, Bakkasb S, Villania G, Varcamontic M, Zanfardinoc A, Gavagnina M (2011) Diterpene content of the alga Dictyota ciliolata from a Moroccan lagoon. Phytochem Lett 2:211–215

    Article  CAS  Google Scholar 

  • Mary JS, Vinotha P, Pradeep AM (2012) Screening for in vitro cytotoxic activity of seaweed, Sargassum sp. against Hep-2 and MCF-7 cancer cell lines. Asian Pac J Cancer Prev 13:6073–6076

    Article  PubMed  Google Scholar 

  • Mayer AMS, Glaser KB, Cuevas C, Jacobs RS, Kem W, Little RD, McIntosh JM, Newman DJ, Potts BC, Shuster DE (2010) The odyssey of marine pharmaceuticals: a current pipeline perspective. Trends Pharmacol Sci 31:255–265

    Article  PubMed  CAS  Google Scholar 

  • Mena-Rejon G, Caamal-Fuentes E, Cantillo-Ciau Z, Cedillo-Rivera R, Flores-Guido J, Moo-Puc R (2009) In vitro cytotoxic activity of nine plants used in Mayan traditional medicine. J Ethnopharmacol 30:462–465

    Article  Google Scholar 

  • Mhadhebi L, Laroche-Clary A, Robert J, Bouraoui A (2011) Antioxidant, anti-inflammatory, and antiproliferative activities of organic fractions from the Mediterranean brown seaweed Cystoseira sedoides. Can J Physiol Pharmacol 89:911–921

    Article  CAS  PubMed  Google Scholar 

  • Moghadam MH, Firouzi J, Saeidnia S, Hajimehdipoor H, Jamili S, Rustaiyan A, Gohari AR (2013) A cytotoxic hydroperoxy sterol from the brown alga, Nizamuddinia zanardinii. Daru J Pharm Sci 21:24

    Article  CAS  Google Scholar 

  • Moo-Puc R, Robledo D, Freile-Pelegrin Y (2008) Evaluation of selected tropical seaweeds for in vitro anti-trichomonal activity. J Ethnopharmacol 30:92–97

    Article  Google Scholar 

  • Moo-Puc R, Robledo D, Freile-Pelegrin Y (2009) In vitro cytotoxic and antiproliferative activities of marine macroalgae from Yucatán, Mexico. Cienc Mar 35:345–358

    CAS  Google Scholar 

  • Nakayasu S, Soegima R, Yamaguchi K, Oda T (2009) biological activities of fucose-containing polysaccharide ascophyllan isolated from the brown alga Ascophyllum nodosum. Biosci Biotechnol Biochem 73:961–964

    Article  PubMed  CAS  Google Scholar 

  • Patarra RF, Leite J, Pereira R, Baptista J, Neto AI (2012) Fatty acid composition of selected macrophytes. Nat Prod Res 27:665–669

    Article  PubMed  CAS  Google Scholar 

  • Pereira DM, Cheel J, Areche C, San-Martin A, Rovirosa J, Silva LR, Valentao P, Andrade PB (2011) Anti-proliferative activity of meroditerpenoids isolated from the brown alga Stypopodium flabelliforme against several cancer cell lines. Mar Drugs 9:852–862

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Pereira H, Barreira L, Figueiredo F, Custódio L, Vizetto-Duarte C, Polo C, Rešek E, Engelen A, Varela J (2012) Polyunsaturated fatty acids of marine macroalgae: potential for nutritional and pharmaceutical applications. Mar Drugs 10:1920–1935

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ponce NM, Pujol CA, Damonte EB, Flores ML, Stortz CA (2003) Fucoidans from the brown seaweed Adenocystis utricularis: extraction methods, antiviral activity and structural studies. Carbohydr Res 338:153–165

    Article  PubMed  CAS  Google Scholar 

  • Rupérez P, Ahrazem O, Leal JA (2002) Potential antioxidant capacity of sulfated polysaccharides from the edible marine brown seaweed Fucus vesiculosus. J Agric Food Chem 50:840–845

    Article  PubMed  CAS  Google Scholar 

  • Sheu JH, Wang GH, Sung PJ, Chiu YH, Duh CY (1997) Cytotoxic sterols from the formosan brown alga Turbinaria ornata. Planta Med 63:571–572

    Article  PubMed  CAS  Google Scholar 

  • Sheu JH, Wang GH, Sung PJ, Duh CY (1999) New cytotoxic oxygenated fucosterols from the brown alga Turbinaria conoides. J Nat Prod 62:224–227

    Article  PubMed  CAS  Google Scholar 

  • Skehan P, Storeng R, Scudiero D, Monks A, McMahon J, Vistica D, Warren JT, Bokesch H, Kenney S, Boyd MR (1990) New colorimetric cytotoxicity assay for anticancer-drug screening. J Natl Cancer Inst 82:1107–1112

    Article  PubMed  CAS  Google Scholar 

  • Stabili L, Acquaviva MI, Biandolino F, Cavallo RA, De Pascali SA, Fanizzi FP, Narracci M, Petrocelli A, Cecere E (2012) The lipidic extract of the seaweed Gracilariopsis longissima (Rhodophyta, Gracilariales): a potential resource for biotechnological purposes? N Biotechnol 29:443–450

    Article  PubMed  CAS  Google Scholar 

  • Teixeira VL, Cavalcanti DN, Pereira RC (2001) Chemotaxonomic study of the diterpenes from the brown alga Dictyota menstrualis. Biochem Syst Ecol 29:313–316

    Article  PubMed  CAS  Google Scholar 

  • Vallim MA, De Paula JC, Pereira RC, Teixeira VL (2005) The diterpenes from Dictyotacean marine brown algae in the tropical Atlantic American region. Biochem Syst Ecol 33:1–16

    Article  CAS  Google Scholar 

  • Viano Y, Bonhomme D, Camps M, Briand JF, Ortalo-Magné A, Blache Y, Piovetti L, Culioli G (2009) Diterpenoids from the Mediterranean brown alga Dictyota sp. evaluated as antifouling substances against a marine bacterial biofilm. J Nat Prod 72:1299–1304

    Article  PubMed  CAS  Google Scholar 

  • Vonthron-Sénécheau C, Bernard-Weniger B, Ouattara M, Tra-Bi F, Kamenan A, Lobstein A, Brun R, Anton R (2003) In vitro antiplasmodial activity and cytotoxicity of ethnobotanically selected Ivorian plants. J Ethnopharmacol 87:221–222

    Article  PubMed  Google Scholar 

  • Wynne MJ (2005) A checklist of benthic marine algae of the tropical andsubtropical western Atlantic: second revision. Nova Hewigia Beih 129:1–152

    Google Scholar 

  • Zubia M, Robledo D, Freile-Pelegrin Y (2007) Antioxidant activities in marine macroalgae from the coasts of Quintana Roo and Yucatan, Mexico. J Appl Phycol 19(5):449–458

    Google Scholar 

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Acknowledgments

The first author acknowledges a postdoctoral fellowship under the research project SEP-CONACYT (CB-83386-Z). The authors thank J.L. Godinez (IB-UNAM) for identification of seaweed species and C. Chávez and M.L. Zaldivar for technical assistance during analysis.

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Authors and Affiliations

  1. Department of Marine Resources, Cinvestav, Unidad Mérida, Mérida, Yucatán, México

    E. Caamal-Fuentes, J. Chale-Dzul, Y. Freile-Pelegrin & D. Robledo

  2. Unidad de Investigación Médica Yucatán, Instituto Mexicano del Seguro Social, Mérida, Yucatán, México

    R. Moo-Puc

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  1. E. Caamal-Fuentes
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  2. J. Chale-Dzul
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  3. R. Moo-Puc
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  4. Y. Freile-Pelegrin
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  5. D. Robledo
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Correspondence to D. Robledo.

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Caamal-Fuentes, E., Chale-Dzul, J., Moo-Puc, R. et al. Bioprospecting of brown seaweed (Ochrophyta) from the Yucatan Peninsula: cytotoxic, antiproliferative, and antiprotozoal activities. J Appl Phycol 26, 1009–1017 (2014). https://doi.org/10.1007/s10811-013-0129-x

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  • DOI: https://doi.org/10.1007/s10811-013-0129-x

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