Antioxidant and Cytotoxic Properties of Two Sea Cucumbers, Holothuria edulis Lesson and Stichopus horrens Selenka

Abstract

Sea cucumbers are marine invertebrates of the phylum of Echinodermata that have been used in Asian traditional medicine since ancient times. This study was conducted to investigate the antioxidant and cytotoxic properties of aqueous and organic extracts from two sea cucumber species, Holothuria edulis Lesson (Holothuriidae) and Stichopus horrens Selenka (Stichopodidae). Antioxidant activities of the extracts were evaluated by DPPH· and β-carotene bleaching assays, while MTT and trypan blue exclusion assays were used to demonstrate the cytotoxic effects of the extracts against two human cancer cell lines, non-small cell lung cancer cells (A549) and esophageal cancer cells (TE1). The results showed that both aqueous and organic extracts of H. edulis were able to scavenge DPPH radical (IC50 at 2.04 mg/ml and 8.73 mg/ml, respectively). Aqueous and organic extracts of S. horrens inhibited 79.62% and 46.66% of β-carotene oxidation by linoleate free radical. On the other hand, the organic extract of S. horrens exhibited the highest cytotoxic effects against A549 and TE1 cancer cells giving IC50 at 15.5 and 4.0 μg/ml, respectively. In conclusion, the present study revealed that H. edulis and S. horrens contain promising levels of antioxidant and cytotoxic natural products that might be used for cancer prevention and treatment.

References

  1. 1.

    Abdille, M., Singh, R., Jayaprakasha, G., Jena, B. (2005) Antioxidant activity of the extracts from Dilleniaindica fruits. Food Chem. 90, 891–896.

    CAS  Article  Google Scholar 

  2. 2.

    Althunibat, O. Y., Ridzwan, B. H., Taher, M., Daud, J. M., Ikeda, M., Zali, B. I. (2009) In vitro antioxidant and antiproliferative activities of three Malaysian sea cucumber species. Eur. J. Sci. Res. 37, 376–387.

    Google Scholar 

  3. 3.

    Andrianasolo, E., McPhail, K., Flatt, R., Gerwick, W. H. (2005) Marine natural products as anticancer drugs. Mol. Cancer Ther. 4, 333–342.

    PubMed  Google Scholar 

  4. 4.

    Blois, M. S. (1958) Antioxidants determination by the use of a stable free radical. Natur. 4617, 1199–1200.

    Article  Google Scholar 

  5. 5.

    Chludil, H. D., Murray, A. R., Seldes, A. M., Maier, M. S. (2003) Biologically active triterpene glycosides from sea cucumbers (Holothuroidea, Echinodermata). In: Atta-ur-Rahman (ed.) Studies in Natural Products Chemistry. Elsevier, Amsterdam, pp. 587–615.

    Google Scholar 

  6. 6.

    Dai, J., Mumpe, R. J. (2010) Plant phenolics: Extraction, analysis and their antioxidant and anticancer properties. Molecule. 15, 7313–7352.

    CAS  Article  Google Scholar 

  7. 7.

    Ehlenfeldt, M. K., Prior, R. L. (2001) Oxygen radical absorbance capacity (ORAC) and phenolic and anthocyanin concentrations in fruit and leaf tissues of highbush blueberry. J. Agric. Food Chem. 49, 2222–2227.

    CAS  Article  Google Scholar 

  8. 8.

    Govindarajan, R., Vrjayakumar, M., Pushpangadan, P. (2005) Antioxidant approach to disease management and the role of ‘Rasayana’ herbs of Ayurveda. J. Ethnopharmacol. 99, 165–178.

    CAS  Article  Google Scholar 

  9. 9.

    Hawa, I., Zulaikah, M., Jamaludin, M., ZainalAbidin, A. A., Kaswandi, M. A., Ridzwan, B. H. (1999) The potential of the coelomic fluid of sea cucumber as an antioxidant. Mal. J. Nutr. 5, 55–59.

    Google Scholar 

  10. 10.

    Husni, A., Shin, I. S., You, S., Chung, D. (2009) Antioxidant properties of water and aqueous ethanol extracts and their crude saponin fractions from a far-eastern sea cucumber, Stichopus japonicus. Food Sci. Biotechnol. 18, 419–424.

    CAS  Google Scholar 

  11. 11.

    Jayaprakasha, G. K., Singh, R. P., Sakariah, K. K. (2001) Antioxidant activity of grape seed (Vitisvinifera) extracts on peroxidation models in vitro. FoodChem. 73, 285–290.

    CAS  Google Scholar 

  12. 12.

    Kaswandi, M. A., Hing, H. L., Sahalan, A. Z., Farah, F., Ridzwan, B. H., Samsudin, M. W., Yasin, M. S. M., Ali, A. (2004) Saponin from sea cucumber Stichopus badionotus Sluiter as potential cytotoxic agent on CEM-SS T-lymphoblastic cell. Annual Conferenc. 4, 112–116.

    Google Scholar 

  13. 13.

    Kumar, A. P., Graham, H., Robson, C., Garapati, K., Ghosh, R. (2011) An overview of anticancer herbal medicines. In: Cho, W. C. S. (ed.) Evidence-based Anticancer Materia Medica. Springer, Dordrecht, Heidelberg, London, New York, pp. 1–36.

    Google Scholar 

  14. 14.

    Longo-Sorbello, G. S. A., Saydam, G., Banerjee, D., Bertino, J. R. (2006) Cytotoxicity and cell growth assays. In: Celis, J. E. (ed.) Cell Biology: A Laboratory Handbook. Elsevier, Amsterdam, pp. 315–324.

    Google Scholar 

  15. 15.

    Mamelona, J., Pelletier, E. M., Lalancette, K. G., Legault, J., Karboune, S., Kermasha, S. (2007) Quantification of phenolic contents and antioxidant capacity of Atlantic sea cucumber. Cucumariafrondosa. Food Chem. 104, 1040–1047.

    CAS  Article  Google Scholar 

  16. 16.

    Moncheva, S., Trakhtenberg, S., Katrichc, E., Zemserd, M., Gosheve, I., Toledof E., Arancibia-Avilaf P., Donchevaa, V., Gorinsteind, S. (2004) Total antioxidant capacity in the black mussel (Mytilusgalloprovincialis) from Black Sea coasts. Estuar. Coast Shelf Sci. 59, 475–484.

    CAS  Article  Google Scholar 

  17. 17.

    Moongkarndi, P., Kosem, N., Kaslungka, S., Luanratana, O., Pongpan, N., Neungton, N. (2004) Antiproliferation, antioxidation and induction of apoptosis by Garciniamangostana (mangosteen) on SKBR3 human breast cancer cell line. J. Ethnopharmacol. 90, 161–166.

    Article  Google Scholar 

  18. 18.

    Ogushi, M., Yoshie-stark, M., Suzuki, T. (2006) Apoptosis-inducing activity of hot water extracts from the sea cucumber in human colon tumor cells. Food Sci. Technol. Res. 12, 290–294.

    Article  Google Scholar 

  19. 19.

    Ridzwan, B. H. (2007) Sea cucumber: The Malaysian Heritage. Research Centre, HUM, Kuala Lumpur, Malaysia.

    Google Scholar 

  20. 20.

    Rodriguez, J., Castro, R., Riguera, R. (1991) Holothurinosides: new anti-tumour non sulphated triter-penoid glycosides from the sea cucumber Holothruiaforskalii.Tetrahedro. 47, 4753–4762.

    CAS  Article  Google Scholar 

  21. 21.

    Sen, S., Chakraborty, R., Sridhar, C., Reddy, Y. S. R., De, B. (2010) Free radicals, antioxidants, diseases and phytomedicines: Current status and future prospect. Int. J. Pharm. Sci. Rev. Res. 3, 93–100.

    Google Scholar 

  22. 22.

    Sugawara, T., Zamia, N., Yamamoto, A., Sakai, S., Noguchi, R., Hiraia, T. (2006) Isolation of sphig-noid bases of sea cucumber cerebrosides and their cytotoxic activity against colon cancer cells. Biosci. Biotechnol. and Biochem. 70, 2906–2912.

    CAS  Article  Google Scholar 

  23. 23.

    Valko, M., Rhodes, C. J., Moncol, J., Izakovic, M., Mazur, M. (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chemico-Biological Interaction. 160, 1–40.

    CAS  Article  Google Scholar 

  24. 24.

    Yang, C. S., Landau, J. M., Huang, M. T., Newmark, H. L. (2001) Inhibition of carcinogenesis by dietary polyphenolic compounds. Annu. Rev. Nutr. 21, 381–406.

    CAS  Article  Google Scholar 

  25. 25.

    Yang, P., Collin, P., Madden, T., Chan, D., Sweeney-Gotsch, B., McConkey, D., Newman, R. A. (2003) Inhibition of proliferation of PC3 cells by the branched-chain fatty acid, 12-methyltetradeca-noic acid, is associated with inhibition of 5-lipoxygenase. Prostat. 55, 281–291.

    CAS  Article  Google Scholar 

  26. 26.

    Zakhari, I. (2003) Determination of cell number. In: Hughes, D., Mehmet, H. (eds) Cell Proliferation & Apoptosis. BIOS Scientific Publishers, Ltd. Oxford, pp. 17–38.

    Google Scholar 

  27. 27.

    Zhong, Y., Ahmad Khan, M., Fereidoon, S. (2007) Compositional characteristics and antioxidant properties of fresh and processed sea cucumber (Cucumariafrondosa). J. Agric. Food Chem. 55, 1188–1192.

    CAS  Article  Google Scholar 

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Acknowledgements

The authors are thankful to the Research Management Center, IIUM for supporting this research (Grant number EDW B 1002-364). Also, we are very grateful to Prof. Dr. Masa-aki Ikeda; Department of Molecular and Carniofacial Embryology, Tokyo Medical and Dental University, for generously providing the cell lines.

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Correspondence to O. Y. Althunibat.

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Althunibat, O.Y., Ridzwan, B.H., Taher, M. et al. Antioxidant and Cytotoxic Properties of Two Sea Cucumbers, Holothuria edulis Lesson and Stichopus horrens Selenka. BIOLOGIA FUTURA 64, 10–20 (2013). https://doi.org/10.1556/ABiol.64.2013.1.2

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Keywords

  • Antioxidant
  • cytotoxic
  • sea cucumber
  • Holothuria edulis
  • Stichopus horrens