Cite this paper:
SILVA J. Paulo, ALVES Celso, PINTEUS Susete, SILVA Joana, VALADO Ana, PEDROSA Rui, PEREIRA Leonel. Antioxidant and antitumor potential of wild and IMTA-cultivated Osmundea pinnatifida[J]. Journal of Oceanology and Limnology, 2019, 37(3): 825-835

Antioxidant and antitumor potential of wild and IMTA-cultivated Osmundea pinnatifida

SILVA J. Paulo1, ALVES Celso2, PINTEUS Susete2, SILVA Joana2, VALADO Ana3, PEDROSA Rui2,4, PEREIRA Leonel5
1 UCIBIO-REQUIMTE, Department of Chemistry, Faculty of Sciences and Technology, Universidade NOVA de Lisboa, Caparica 2829-516, Portugal;
2 MARE-Marine and Environmental Sciences Centre, School of Tourism and Maritime Technology, Polytechnic Institute of Leiria, Peniche 2520-641, Portugal;
3 Instituto Politécnico de Coimbra, ESTESC-Coimbra Health School, Biomedical Sciences Laboratory, R. 5 de Outubro, S. Martinho do Bispo, Ap. 7006, Coimbra 3046-854, Portugal;
4 Centre of Pharmacology and Chemical Biopathology, Faculty of Medicine, University of Porto, Porto 4200-319, Portugal;
5 MARE-Marine and Environmental Sciences Centre, Department of Life Sciences, Faculty of Sciences and Technology, University of Coimbra, Coimbra 3000-456, Portugal
Abstract:
Osmundea pinnatifida is a red edible seaweed known as pepper dulse. O. pinnatifida was cultivated in the farm of ALGAplus (Ílhavo, Portugal). This farm is integrated with a seabream and seabass commercial aquaculture and uses the nutrient-enriched water resultant from the fish production as its cultivation medium in the integrated multi-trophic aquaculture (IMTA) manner. Wild and IMTA-cultivated samples of O. pinnatifida were screened for antioxidant and antitumor activities. The antioxidant capacity of solvent extracts from wild and IMTA cultivated samples was assessed in two methods (2,2-diphenyl-1-picrylhydrazyl (DPPH) and oxygen radical absorbance capacity (ORAC)), and their total phenolic contents (TPC) were estimated. Antitumor activity was evaluated in three different tumor cell lines (HepG-2, MCF-7, and SH-SY5Y) through 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay. Among the solvents used for extraction, dichloromethane was the most effective to extract phenolic compounds and presented higher ORAC. A significant correlation was found between TPC and ORAC, which was also sustained by the principal components analysis (PCA). Dichloromethane extracts induced a cytostatic effect on MCF-7 cells and showed weak cytotoxicity to SH-SY5Y cells and weak impact on cell proliferation. Overall, there were no statistically significant differences in the biological activities shown by the wild and IMTA-cultivated samples. Hence, O. pinnatifida can be obtained in an economical and environmentally sustainable way through IMTA, maintaining bioactive properties in a high potential for further nutraceutical purposes.
Key words:    edible seaweed|bioactive compounds|polyphenols|cytotoxic activity|antiproliferative activity   
Received: 2018-05-21   Revised: 2018-07-31
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Articles by SILVA J. Paulo
Articles by ALVES Celso
Articles by PINTEUS Susete
Articles by SILVA Joana
Articles by VALADO Ana
Articles by PEDROSA Rui
Articles by PEREIRA Leonel
References:
Abreu M H, Pereira R, Yarish C, Buschmann A H, Sousa-Pinto I. 2011. IMTA with Gracilaria vermiculophylla:productivity and nutrient removal performance of the seaweed in a landbased pilot scale system. Aquaculture, 312(1-4):77-87, https://doi.org/10.1016/j.aquaculture.2010.12.036.
Abu-Dahab R, Afifi F. 2007. Antiproliferative activity of selected medicinal plants of Jordan against a breast adenocarcinoma cell line (MCF7). Scientia Pharmaceutica, 75(3):121-136, https://doi.org/10.3797/scipharm.2007.75.121.
Airanthi M K W A, Hosokawa M, Miyashita K. 2011.Comparative antioxidant activity of edible Japanese brown seaweeds. Journal of Food Science, 76(1):C104-C111, https://doi.org/10.1111/j.1750-3841.2010.01915.x.
Alves C, Pinteus S, Horta A, Pedrosa R. 2016. High cytotoxicity and anti-proliferative activity of algae extracts on an in vitro model of human hepatocellular carcinoma. SpringerPlus, 5(1):1 339, https://doi.org/10.1186/s40064-016-2938-2.
American Cancer Society. 2018. Cancer facts & figures 2018.https://www.cancer.org/content/dam/cancer-org/research/cancer-facts-and-statistics/annual-cancer-facts-and-figures/2018/cancer-facts-and-figures-2018.pdf. Accessed on 2018-02-10.
Bae H, Jayaprakasha G K, Crosby K, Jifon J L, Patil B S. 2012.Influence of extraction solvents on antioxidant activity and the content of bioactive compounds in non-pungent peppers. Plant Foods for Human Nutrition, 67(2):120-128, https://doi.org/10.1007/s11130-012-0290-4.
Barreto M C, Mendonça E, Gouveia V, Anjos C, Medeiros J S, Seca A M L, Neto A I. 2012. Macroalgae from S. Miguel Island as a potential source of antiproliferative and antioxidant products. Arquipelago Life Mar. Sci., 29:53-58.
Bedoux G, Hardouin K, Burlot A S, Bourgougnon N. 2014.Bioactive components from seaweeds:cosmetic applications and future development. Advances in Botanical Research, 71:345-378.
Burtin P. 2003. Nutritional value of seaweeds. Electron. J.Environ. Agric. Food Chem., 2:498-503.
Cardoso S M, Carvalho L G, Silva P J, Rodrigues M S, Pereira O R, Pereira L. 2014. Bioproducts from seaweeds:a review with special focus on the Iberian Peninsula.Current Organic Chemistry, 18(7):896-917, https://doi.org/10.2174/138527281807140515154116.
Dai J, Mumper R J. 2010.Plant phenolics:extraction, analysis and their antioxidant and anticancer properties.Molecules, 15(10):7 313-7 352, https://doi.org/10.3390/molecules15107313.
Dávalos A, Gómez-Cordovés C, Bartolomé B. 2004. Extending applicability of the oxygen radical absorbance capacity(ORAC-fluorescein) assay. Journal of Agricultural and Food Chemistry, 52(1):48-54, https://doi.org/10.1021/jf0305231.
De Quirós A R B, Lage-Yusty M A, López-Hernández J. 2010.Determination of phenolic compounds in macroalgae for human consumption. Food Chemistry, 121(2):634-638, https://doi.org/10.1016/j.foodchem.2009.12.078.
Foo SC, Yusoff F M, Ismail M, Basri M, Yau S K, Khong M H, Chan K W, Ebrahimi M. 2017. Antioxidant capacities of fucoxanthin-producing algae as influenced by their carotenoid and phenolic contents. Journal of Biotechnology, 241:175-183, https://doi.org/10.1016/j.jbiotec.2016.11.026.
Ganesan P, Kumar C S, Bhaskar N. 2008. Antioxidant properties of methanol extract and its solvent fractions obtained from selected Indian red seaweeds. Bioresource Technology, 99(8):2 717-2 723, https://doi.org/10.1016/j.biortech.2007.07.005.
GBD 2015 Mortality and Causes of Death Collaborators. 2016. Global, regional, and national life expectancy, allcause mortality, and cause-specific mortality for 249 causes of death, 1980-2015:a systematic analysis for the Global Burden of Disease Study 2015. Lancet, 388(10053):1 459-1 544, https://doi.org/10.1016/S0140-6736(16)31012-1.
Herald T J, Gadgil P, Tilley M. 2012. High-throughput micro plate assays for screening flavonoid content and DPPHscavenging activity in sorghum bran and flour. Journal of the Science of Food and Agriculture, 92(11):2 326-2 331, https://doi.org/10.1002/jsfa.5633.
Holdt S L, Kraan S. 2011. Bioactive compounds in seaweed:functional food applications and legislation. Journal of Applied Phycology, 23(3):543-597, https://doi.org/10.1007/s10811-010-9632-5.
Huang D J, Ou B X, Prior R L. 2005. The chemistry behind antioxidant capacity assays. Journal of Agricultural and Food Chemistry, 53(6):1 841-1 856, https://doi.org/10.1021/jf030723c.
Ibañez E, Herrero M, Mendiola JA, Castro-Puyana M. 2012.Extraction and characterization of bioactive compounds with health benefits from marine resources:macro and micro algae, cyanobacteria, and invertebrates. In:Hayes M ed. Marine Bioactive Compounds. Springer US, Boston, MA. p.55-98.
Ito K, Hori K. 1989. Seaweed:chemical composition and potential food uses. Food Reviews International, 5(1):101-144, https://doi.org/10.1080/87559128909540845.
Juagdan E G, Kalidindi R, Scheuer P. 1997. Two new chamigranes from an hawaiian red alga, Laurencia cartilaginea. Tetrahedron, 53(2):521-528, https://doi.org/10.1016/S0040-4020(96)01002-2.
Lee J C, Hou M F, Huang H W, Chang F R, Yeh C C, Tang J Y, Chang H W. 2013. Marine algal natural products with anti-oxidative, anti-inflammatory, and anti-cancer properties. Cancer Cell International, 13:55, https://doi.org/10.1186/1475-2867-13-55.
Lesjak M, Beara I, Simin N, Pintać D, Majkić T, Bekvalac K, Orčić D, Mimica-Dukić N. 2018. Antioxidant and antiinflammatory activities of quercetin and its derivatives.Journal of Functional Foods, 40:68-75, https://doi.org/10.1016/j.jff.2017.10.047.
Liu Z, Romero-Canelón I, Qamar B, Hearn J M, Habtemariam A, Barry N P E, Pizarro A M, Clarkson G J, Sadler P J. 2014. The potent oxidant anticancer activity of organoiridium catalysts. Angew Chemie, 53(15):3 941-3 946, https://doi.org/10.1002/anie.201311161.
Martins A, Vieira H, Gaspar H, Santos S. 2014. Marketed marine natural products in the pharmaceutical and cosmeceutical industries:tips for success. Marine Drugs, 12(2):1 066-1 101, https://doi.org/10.3390/md12021066.
Murphy C, Hotchkiss S, Worthington J, McKeown S R. 2014.The potential of seaweed as a source of drugs for use in cancer chemotherapy. Journal of Applied Phycology, 26(5):2 211-2 264, https://doi.org/10.1007/s10811-014-0245-2.
Nogueira C C, Paixão I C, Teixeira V L. 2014. Antioxidant activity of natural products isolated from red seaweeds.Natural Product Communications, 9(7):1 031-1 036.
Norte M, Fernández J J, Souto M L, Gavín J A, García-Grávalos M D. 1997. Thyrsenols A and B, two unusual polyether squalene derivatives. Tetrahedron, 53(9):3 173-3 178, https://doi.org/10.1016/S0040-4020(97)00028-8.
Paiva L S, Patarra R F, Neto A I, Emc L, Jab B. 2012.Antioxidant activity of macroalgae from the Azores.Arquipelago Life Mar. Sci., 29:1-6.
Paiva L, Lima E, Patarra R F, Neto A I, Baptista J. 2014. Edible Azorean macroalgae as source of rich nutrients with impact on human health. Food Chemistry, 164:128-135, https://doi.org/10.1016/j.foodchem.2014.04.119.
Pangestuti R, Kim S K. 2011. Neuroprotective effects of marine algae. Marine Drugs, 9(5):803-818.
Park E J, Pezzuto J M. 2013. Antioxidant marine products in cancer chemoprevention. Antioxidants & Redox Signaling, 19(2):115-138, https://doi.org/10.1089/ars.2013.5235.
Patarra R F, Leite J, Pereira R, Baptista J, Neto A I. 2013. Fatty acid composition of selected macrophytes. Natural Product Research, 27(7):665-669, https://doi.org/10.1080/14786419.2012.688048.
Pereira L. 2016. Edible Seaweeds of the World. Science Publishers' (SP), an Imprint of CRC Press/Taylor & Francis Group, Boca Raton, FL. 448p.
Pereira L. 2018. Therapeutic and Nutritional Uses of Algae.CRC PressBoca Raton, FL. 640p.
Pinteus S, Silva J, Alves C, Horta A, Thomas O P, Pedrosa R. 2017. Antioxidant and cytoprotective activities of fucus spiralis seaweed on a human cell in vitro model.International Journal of Molecular Sciences, 18(2):292, https://doi.org/10.3390/ijms18020292.
Pomponi S A. 2001. Roger revelle commemorative lecture-the oceans and human health:the discovery and development of marine-derived drugs. Oceanography, 14(1):78-87.
Rodrigues D, Freitas A C, Pereira L, Rocha-Santos T A P, Vasconcelos M W, Roriz M, Rodríguez-Alcalá L M, Gomes A M P, Duarte A C. 2015b. Chemical composition of red, brown and green macroalgae from Buarcos bay in Central West Coast of Portugal. Food Chemistry, 183:197-207, https://doi.org/10.1016/j.foodchem.2015.03.057.
Rodrigues D, Sousa S, Silva A, Amorim M, Pereira L, RochaSantos T A P, Gomes A M P, Duarte A C, Freitas A C. 2015a. Impact of enzyme- and ultrasound-assisted extraction methods on biological properties of red, brown, and green seaweeds from the central west coast of Portugal. Journal of Agricultural and Food Chemistry, 63(12):3 177-3 188, https://doi.org/10.1021/jf504220e.
Rodrigues D, Walton G, Sousa S, Rocha-Santos T A P, Duarte A C, Freitas A C, Gomes A M P. 2016. In vitro fermentation and prebiotic potential of selected extracts from seaweeds and mushrooms. LWT, 73:131-139, https://doi.org/10.1016/j.lwt.2016.06.004.
Sathya R, Kanaga N, Sankar P, Jeeva S. 2017. Antioxidant properties of phlorotannins from brown seaweed Cystoseira trinodis (Forsskål) C. Agardh. Arabian Journal of Chemistry, 10(S2):S2 608-S2 614, https://doi.org/10.1016/j.arabjc.2013.09.039.
Silva P J, Alves C, Pinteus S, Silva J, Valado A, Pedrosa R, Pereira L. 2017. Screening of Biotechnological Potential of wild and IMTA-Cultivated Osmundea Pinnatifida(Rhodophyta). P1. 33, 7th International Conference on Algal Biomass, Biofuels & Bioproducts. 18-21 June 2017, Miami, FL.
Smit A J. 2004. Medicinal and pharmaceutical uses of seaweed natural products:a review. Journal of Applied Phycology, 16(4):245-262, https://doi.org/10.1023/B:JAPH. 0000047783.36600.ef.
Sudha A, Jeyakanthan J, Srinivasan P. 2017. Green synthesis of silver nanoparticles using Lippia nodiflora aerial extract and evaluation of their antioxidant, antibacterial and cytotoxic effects. Resource-Efficient Technologies, 3(4):506-515, https://doi.org/10.1016/j.reffit.2017.07.002.
Tsimberidou A M. 2015. Targeted therapy in cancer. Cancer Chemotherapy and Pharmacology, 76(6):1 113-1 132, https://doi.org/10.1007/s00280-015-2861-1.
Wang T, Jónsdóttir R, Ólafsdóttir G. 2009. Total phenolic compounds, radical scavenging and metal chelation of extracts from Icelandic seaweeds. Food Chemistry, 116(1):240-248, https://doi.org/10.1016/j.foodchem. 2009.02.041.
Wojcikowski K, Stevenson L M, Leach D N, Wohlmuth H, Gobe G. 2007. Antioxidant capacity of 55 medicinal herbs traditionally used to treat the urinary system:a comparison using a sequential three-solvent extraction process.Journal of Alternative and Complementary Medicine, 13(1):103-109, https://doi.org/10.1089/acm.2006.6122.
Zou Y P, Chang S K C, Gu Y, Qian S Y. 2011. Antioxidant activity and phenolic compositions of lentil (Lens culinaris var. Morton) extract and its fractions. Journal of Agricultural & Food Chemistry, 59(6):2 268-2 276, https://doi.org/10.1021/jf104640k.
Zulueta A, Esteve M J, Frígola A. 2009. ORAC and TEAC assays comparison to measure the antioxidant capacity of food products. Food Chemistry, 114(1):310-316, https://doi.org/10.1016/j.foodchem.2008.09.033.
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