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Articles

Red seaweeds Porphyra umbilicalis and Grateloupia turuturu display antigenotoxic and longevity-promoting potential in Drosophila melanogaster

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Pages 519-530 | Received 07 Oct 2018, Accepted 19 Mar 2019, Published online: 15 Jul 2019

References

  • Abraham, S.K. (1994). Antigenotoxicity of coffee in the Drosophila assay for somatic mutation and recombination. Mutagenesis, 9: 383–386.
  • Baweja, P., Kumar, S., Sahoo, D. & Levine, I. (2016). Biology of seaweeds. In Seaweed in Health and Disease Prevention (Fleurence, J. & Levine, I., editors), 41–106. Academic Press, London.
  • Bixler, H.J. & Porse, H. (2011). A decade of change in the seaweed hydrocolloids industry. Journal of Applied Phycology, 23: 321–335.
  • Bolzán, A.D. & Bianchi, M.S. (2001). Genotoxicity of streptonigrin: a review. Mutation Research, 488: 25–37.
  • Brawley, S.H., Blouin, N.A., Ficko-Blean, E., Wheeler, G., Lohr, M., Goodson, H.V., Jenkins, J., Blaby-Haas, C.E., Helliwell, K., Chan, C.X., Marriage, T., Bhattacharya, D., Klein, A., Badis, Y., Brodie, J., Cao, Y., Collen, J., Dittami, S., Gachon, C., Green, B., Karpowicz, S., Kim, J., Lin, S., Michel, G., Mittag, M., Olson, B., Pangilinan, J., Peng, Y., Qiu, H., Riek, S.Z., Shu, S.Q., Singer, J., Smith, A., Sprecher, B., Wagner, V., Wang, W., Wang, Z., Yan, Z., Yarish, C., Zhuang, Y.Y., Zou, Y., Lindquist, E., Grimwood, J., Barry, K., RoksharD., Schumtz, J., Gantt, E., Stiller, J., Grossman, A., Prochnik, S. (2017). Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta). Proceedings of the National Academy of Sciences USA, 114: E6361–E6370.
  • Cofrades, S., López-López, I., Bravo, L., Ruiz-Capillas, C., Bastida, S., Larrea, M.T. & Jiménez-Colmenero, F. (2010). Nutritional and antioxidant properties of different brown and red Spanish edible seaweeds. Food Science and Technology International, 16: 361–370.
  • Collins, K.G., Fitzgerald, G.F., Stanton, C. & Ross, R.P. (2016). Looking beyond the terrestrial: the potential of seaweed derived bioactives to treat non-communicable diseases. Marine Drugs, 14: 1–31.
  • Corato, U.D., Salimbeni, R., Pretis, A.D., Avella, N. & Patruno, G. (2017). Antifungal activity of crude extracts from brown and red seaweeds by a supercritical carbon dioxide technique against fruit postharvest fungal diseases. Postharvest Biology and Technology, 131: 16–30.
  • Couteau, C. & Coiffard, L. (2016). Seaweed application in cosmetics. In Seaweed in Health and Disease Prevention (Fleurence, J. & Levine, I., editors), 423–441. Academic Press, London.
  • Dawes, C. (2016). Macroalgae systematics. In Seaweed in Health and Disease Prevention (Fleurence, J. & Levine, I., editors), 107–148. Academic Press, London.
  • Deepa, P.V., Akshaya, A.S. & Solomon, F.D.P. (2011). Anthracycline (epirubicin) induced mutation studies in Drosophila melanogaster. Drosophila Information Service, 94: 53–61.
  • Demir, E., Kaya, B. & Cenkci, S.K. (2013). Antigenotoxic activities of ascorbic acid, chlorophyll a, and chlorophyll b in acrolein and malondialdehyde-induced genotoxicity in Drosophila melanogaster. Ekoloji, 22: 36–42.
  • Denis, C., Morançais, M., Li, M., Deniaud, E., Gaudin, P., Wielgosz-Collin, G., Barnathan, G., Jaouen, P. & Fleurence, J. (2010). Study of the chemical composition of edible red macroalgae Grateloupia turuturu from Brittany (France). Food Chemistry, 119: 913–917.
  • Dias, C.D., Araújo, B.C., Dutra, E.S. & Nepomuceno, J.C. (2009). Protective effects of β-carotene against the genotoxicity of doxorubicin in somatic cells of Drosophila melanogaster. Genetics and Molecular Research, 8: 1367–1375.
  • Donohoe, T.J., Jones, C.R., Kornahrens, A.F., Barbosa, L.C.A., Walport, L.J., Tatton, M.R., O’Hagan, M., Rathi, A.H. & Baker, D.B. (2013). Total synthesis of the antitumor antibiotic (±)-streptonigrin: first- and second-generation routes for de novo pyridine formation using ring-closing metathesis. Journal of Organic Chemistry, 78: 12338–12350.
  • Driver, C. & Georgeou, A. (2003). Variable effects of vitamin E on Drosophila longevity. Biogerontology, 4: 91–95.
  • Edifizi, D. & Schumacher, B. (2015). Genome instability in development and aging: insights from nucleotide excision repair in humans, mice, and worms. Biomolecules, 5: 1855–1869.
  • Ekaterina, L., Ekaterina, P., Svetlana, Z., Oksana, S., Elena, M., Sergey, L., Alex, M., Alex, Z. & Alexey, M. (2015). Fucoxanthin increases lifespan of Drosophila melanogaster and Caenorhabditis elegans. Pharmacological Research, 100: 228–241.
  • FAO (2016). The State of World Fisheries and Aquaculture 2016. FAO, Rome.
  • Fernández-Bedmar, Z., Anter, J., Cruz-Ares, S.L., Muñoz-Serrano, A., Alonso-Moraga, Á. & Pérez-Guisado, J. (2011). Role of citrus juices and distinctive components in the modulation of degenerative processes: genotoxicity, antigenotoxicity, cytotoxicity, and longevity in Drosophila. Journal of Toxicology and Environmental Health, Part A, 74: 1052–1066.
  • Ferraces-Casais, P., Lage-Yusty, M.A., Quirós, A.R.-B.d., & López-Hernández, J. (2012). Evaluation of bioactive compounds in fresh edible seaweeds. Food Analytical Methods, 5: 828–834.
  • Fleurence, J., Gutbier, G., Mabeau, S. & Leray, C. (1994). Fatty acids from 11 marine macroalgae of the French Brittany coast. Journal of Applied Phycology, 6: 527–532.
  • Franke, T.M., Ho, T. & Christie, C.A. (2012). The chi-square test: often used and more often misinterpreted. American Journal of Evaluation, 33: 448–458.
  • Frei, H. & Würgler, F.E. (1988). Statistical methods to decide whether mutagenicity test data from Drosophila assays indicate a positive, negative, or inconclusive result. Mutation Research, 203: 297–308.
  • Gaivão, I. & Comendador, M.A. (1996). The w/w+ somatic mutation and recombination test (SMART) of Drosophila melanogaster for detecting reactive oxygen species: characterization of 6 strains. Mutation Research, 360: 145–151.
  • Gaivão, I., Sierra, L.M. & Comendador, M.A. (1999). The w/w+ SMART assay of Drosophila melanogaster detects the genotoxic effects of reactive oxygen species inducing compounds. Mutation Research, 440: 139–145.
  • García-Bueno, N., Decottignies, P., Turpin, V., Dumay, J., Paillard, C., Stiger-Pouvreau, V., Kervarec, N., Pouchus, Y.-F., Marín-Atucha, A.A. & Fleurence, J. (2014). Seasonal variation in the antivibrio activity of two organic extracts from two red seaweed: Palmaria palmata and the introduced Grateloupia turuturu against the abalone pathogen Vibrio harveyi. Aquatic Living Resources, 27: 83–89.
  • Genova, M.L. & Lenaz, G. (2015). The interplay between respiratory supercomplexes and ROS in aging. Antioxidants & Redox Signaling, 23: 208–238.
  • Govindaraju, D., Atzmon, G. & Barzilai, N. (2015). Genetics, lifestyle and longevity: lessons from centenarians. Applied and Translational Genomics, 4: 23–32.
  • Graf, U., Würgler, F.E., Katz, A.J., Frei, H., Juon, H., Hall, C.B., & Kale, P.G. (1984). Somatic mutation and recombination test in Drosophila melanogaster. Environmental Mutagenesis, 6: 153–188.
  • Graf, U., Abraham, S.K., Guzman-Rincon, J. & Würgler, F.E. (1998). Antigenotoxicity studies in Drosophila melanogaster. Mutation Research, 402: 203–209.
  • Guinea, M., Franco, V., Araujo-Bazán, L., Rodríguez-Martín, I. & González, S. (2012). In vivo UVB-photoprotective activity of extracts from commercial marine macroalgae. Food and Chemical Toxicology, 50: 1109–1117.
  • Han, S.K., Lee, D., Lee, H., Kim, D., Son, H.G., Yang, J.-S., Lee, S.-J.V. & Kim, S. (2016). OASIS 2: online application for survival analysis 2 with features for the analysis of maximal lifespan and healthspan in aging research. Oncotarget, 7: 56147–56152.
  • Holdt, S.L. & Kraan, S. (2011). Bioactive compounds in seaweed: functional food applications and legislation. Journal of Applied Phycology, 23: 543–597.
  • Holmes, A.M., Creton, S. & Chapman, K. (2010). Working in partnership to advance the 3Rs in toxicity testing. Toxicology, 267: 14–19.
  • Hudson, J.B., Kim, J.H., Lee, M.K., DeWreede, R.E. & Hong, Y.K. (1999). Antiviral compounds in extracts of Korean seaweeds: evidence for multiple activities. Journal of Applied Phycology, 10: 427–434.
  • Jiménez-Escrig, A., Jiménez-Jiménez, I., Pulido, R. & Saura-Calixto, F. (2001). Antioxidant activity of fresh and processed edible seaweeds. Journal of the Science of Food and Agriculture, 81: 530–534.
  • Kaplan, E.L. & Meier, P. (1958). Nonparametric estimation from incomplete observations. Journal of the American Statistical Association, 53: 457–481.
  • Kendel, M., Couzinet-Mossion, A., Viau, M., Fleurence, J., Barnathan, G. & Wielgosz-Collin, G. (2013). Seasonal composition of lipids, fatty acids, and sterols in the edible red alga Grateloupia turuturu. Journal of Applied Phycology, 25: 425–432.
  • Kraan, S. (2016). Seaweed and alcohol: biofuel or booze? In Seaweed in Health and Disease Prevention (Fleurence, J. & Levine, I., editors), 169–184. Academic Press, London.
  • Lemaitre, B. & Miguel-Aliaga, I. (2013). The digestive tract of Drosophila melanogaster. Annual Review of Genetics, 47: 377–404.
  • Levine, I. (2016). Algae: a way of life and health. In Seaweed in Health and Disease Prevention (Fleurence, J. & Levine, I., editors), 1–5. Academic Press, London.
  • Liu, F. & Pang, S.J. (2010). Stress tolerance and antioxidant enzymatic activities in the metabolisms of the reactive oxygen species in two intertidal red algae Grateloupia turuturu and Palmaria palmata. Journal of Experimental Marine Biology and Ecology, 382: 82–87.
  • MacArtain, P., Gill, C.I.R., Brooks, M., Campbell, R. & Rowland, I.R. (2007). Nutritional value of edible seaweeds. Nutrition Reviews, 65: 535–543.
  • Mann, H.B. & Whitney, D.R. (1947). On a test of whether one of two random variables is stochastically larger than the other. Annals of Mathematical Statistics, 18: 50–60.
  • Mantel, N. (1966). Evaluation of survival data and two new rank order statistics arising in its consideration. Cancer Chemotherapy Reports, 50: 163–170.
  • Marcos, R., Sierra, L.M. & Gaivão, I. (2014). The SMART assays of Drosophila: wings and eyes as target tissues. In Genotoxicity and DNA Repair: A Practical Approach (Sierra, L.M. & Gaivão, I., editors), 283–295. Humana Press, New York.
  • Marsham, S., Scott, G.W. & Tobin, M.L. (2007). Comparison of nutritive chemistry of a range of temperate seaweeds. Food Chemistry, 100: 1331–1336.
  • McKinnon, P.J. (2017). Genome integrity and disease prevention in the nervous system. Genes and Development, 31: 1180–1194.
  • Mendis, E. & Kim, S.-K. (2011). Present and future prospects of seaweeds in developing functional foods. Advances in Food and Nutrition Research, 64: 1–15.
  • Mishra, N., Srivastava, R., Agrawal, U.R. & Tewari, R.R. (2017). An insight into the genotoxicity assessment studies in dipterans. Mutation Research, 773: 220–229.
  • Mohamed, S., Hashim, S.N. & Rahman, H.A. (2012). Seaweeds: a sustainable functional food for complementary and alternative therapy. Trends in Food Science and Technology, 23: 83–96.
  • Morrissey, J., Kraan, S. & Guiry, M.D. (2001). A Guide to Commercially Important Seaweeds on the Irish Coast. Bord Iascaigh Mhara, Dublin.
  • Munier, M., Dumay, J., Morançais, M., Jaouen, P. & Fleurence, J. (2013). Variation in the biochemical composition of the edible seaweed Grateloupia turuturu Yamada harvested from two sampling sites on the Brittany Coast (France): the influence of storage method on the extraction of the seaweed pigment R-phycoerythrin. Journal of Chemistry, 2013: 1–8.
  • Ong, C., Yung, L.-Y.L., Cai, Y., Bay, B.-H. & Baeg, G.-H. (2014). Drosophila melanogaster as a model organism to study nanotoxicity. Nanotoxicology, 9: 396–403.
  • Oucif, H., Adjout, R., Sebahi, R., Boukortt, F.O., Ali-Mehidi, S. & Abi-Ayad, S.-M.E.-A. (2017). Comparison of in vitro antioxidant activity of some selected seaweeds from Algerian West Coast. African Journal of Biotechnology, 16: 1474–1480.
  • Pan, M.-H., Lai, C.-S., Tsai, M.-L., Wu, J.-C. & Ho, C.-T. (2012). Molecular mechanisms for anti-aging by natural dietary compounds. Molecular Nutrition and Food Research, 56: 88–115.
  • Pang, S.J., Xiao, T., Shan, T.F., Wang, Z.F. & Gao, S.Q. (2006). Evidences of the intertidal red alga Grateloupia turuturu in turning Vibrio parahaemolyticus into non-culturable state in the presence of light. Aquaculture, 260: 369–374.
  • Panieri, E. & Santoro, M.M. (2016). ROS homeostasis and metabolism: a dangerous liason in cancer cells. Cell Death and Disease, 7: e2253.
  • Peinado, I., Girón, J., Koutsidis, G. & Ames, J.M. (2014). Chemical composition, antioxidant activity and sensory evaluation of five different species of brown edible seaweeds. Food Research International, 66: 36–44.
  • Pereira, L. (2015). Seaweed flora of the European North Atlantic and Mediterranean. In Handbook of Marine Biotechnology (Kim, S.-K., editor), 65–178. Springer, Berlin.
  • Plouguerné, E., Hellio, C., Deslandes, E., Véron, B. & Stiger-Pouvreau, V. (2008). Anti-microfouling activities in extracts of two invasive algae: Grateloupia turuturu and Sargassum muticum. Botanica Marina, 51: 202–208.
  • Qin, Y. (2018). Applications of bioactive seaweed substances in functional food products. In Bioactive Seaweeds for Food Applications: Natural Ingredients for Healthy Diets (Qin, Y., editor), 111–132. Academic Press, London.
  • Rizki, M., Amrani, S., Creus, A., Xamena, N. & Marcos, R. (2001). Antigenotoxic properties of selenium: studies in the wing spot test in Drosophila. Environmental and Molecular Mutagenesis, 37: 70–75.
  • 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. (2015a). Chemical composition of red, brown and green macroalgae from Buarcos bay in Central West Coast of Portugal. Food Chemistry, 183: 197–207.
  • Rodrigues, M.A., Martins, N.E., Balancé, L.F., Brooma, L.N., Dias, A.J.S., Fernandes, A.S.D., Rodrigues, F., Sucena, É. & Mirth, C.K. (2015b). Drosophila melanogaster larvae make nutritional choices that minimize developmental time. Journal of Insect Physiology, 81: 69–80.
  • Rupérez, P. & Saura-Calixto, F. (2001). Dietary fibre and physicochemical properties of edible Spanish seaweeds. European Food Research and Technology, 212: 349–354.
  • Rupérez, P., Ahrazem, O. & Leal, J.A. (2002). Potential antioxidant capacity of sulfated polysaccharides from the edible marine brown seaweed Fucus vesiculosus. Journal of Agricultural and Food Chemistry, 50: 840–845.
  • Sampath-Wiley, P., Neefus, C.D. & Jahnke, L.S. (2008). Seasonal effects of sun exposure and emersion on intertidal seaweed physiology: fluctuations in antioxidant contents, photosynthetic pigments and photosynthetic efficiency in the red alga Porphyra umbilicalis Kützing (Rhodophyta, Bangiales). Journal of Experimental Marine Biology and Ecology, 361: 83–91.
  • Sánchez-Machado, D.I., López-Cervantes, J., López-Hernández, J. & Paseiro-Losada, P. (2004). Fatty acids, total lipid, protein and ash contents of processed edible seaweeds. Food Chemistry, 85: 439–444.
  • Sarıkaya, R., Erciyas, K., Kara, M.I., Sezer, U., Erciyas, A.F. & Ay, S. (2016). Evaluation of genotoxic and antigenotoxic effects of boron by the somatic mutation and recombination test (SMART) on Drosophila. Drug and Chemical Toxicology, 39: 400–406.
  • Selby, P.B. & Olson, W.H. (1981). Methods and criteria for deciding whether specific-locus mutation-rate data in mice indicate a positive, negative or inconclusive result. Mutation Research, 83: 403–418.
  • Shanmugam, M. & Mody, K.H. (2000). Heparinoid-active sulphated polysaccharides from marine algae as potential blood anticoagulant agents. Current Science, 79: 1672–1683.
  • Silva, M., Vieira, L., Almeida, A.P. & Kijjoa, A. (2013). The marine macroalgae of the genus Ulva: chemistry, biological activities and potential applications. Oceanography, 1: 1–6.
  • Soh, J.-W., Marowsky, N., Nichols, T.J., Rahman, A.M., Miah, T., Sarao, P., Khasawneh, R., Unnikrishnan, A., Heydari, A.R., Silver, R.B. & Arking, R. (2013). Curcumin is an early-acting stage-specific inducer of extended functional longevity in Drosophila. Experimental Gerontology, 48: 229–239.
  • Stamenković-Radak, M. & Andjelković, M. (2016). Studying genotoxic and antimutagenic effects of plant extracts in Drosophila test systems. Botanica Serbica, 40: 21–28.
  • Troxell, B., Xu, H. & Yang, X.F. (2012). Borrelia burgdorferi, a pathogen that lacks iron, encodes manganese-dependent superoxide dismutase essential for resistance to streptonigrin. Journal of Biological Chemistry, 287: 19284–19293.
  • Vogel, E.W. & Nivard, M.J.M. (1993). Performance of 181 chemicals in a Drosophila assay predominantly monitoring interchromosomal mitotic recombination. Mutagenesis, 8: 57–81.
  • Vogel, E.W. & Zijlstra, J.A. (1987). Mechanistic and methodological aspects of chemically induced somatic mutation and recombination in Drosophila melanogaster. Mutation Research, 182: 243–264.
  • Wang, C., Li, Q., Redden, D.T., Weindruch, R. & Allison, D.B. (2004). Statistical methods for testing effects on “maximum lifespan”. Mechanisms of Ageing and Development, 125: 629–632.
  • Yang, J.-S., Nam, H.-J., Seo, M., Han, S.K., Choi, Y., Nam, H.G., Lee, S.-J. & Kim, S. (2011). OASIS: online application for the survival analysis of lifespan assays performed in aging research. PLoS ONE, 6: e23525.
  • Zhang, Z., Han, S., Wang, H. & Wang, T. (2014). Lutein extends the lifespan of Drosophila melanogaster. Archives of Gerontology and Geriatrics, 58: 153–159.
  • Zhao, T., Zhang, Q., Qi, H. & Li, Z. (2007). Positive effect of porphyrans on the lifespan and vitality of Drosophila melanogaster. Chinese Journal of Oceanology and Limnology, 25: 373–377.
  • Zhao, T., Zhanga, Q., Qic, H., Liud, X. & Li, Z. (2008). Extension of life span and improvement of vitality of Drosophila melanogaster by long-term supplementation with different molecular weight polysaccharides from Porphyra haitanensis. Pharmacological Research, 57: 67–72.

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