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Marine Biotechnology

, Volume 13, Issue 2, pp 205–214 | Cite as

The Effect of Ultrasonificated Extracts of Spirulina maxima on the Anticancer Activity

  • Sung-Ho Oh
  • Juhee Ahn
  • Do-Hyung Kang
  • Hyeon-Yong Lee
Original Article

Abstract

The effect of ultrasonic extraction on extraction yields, cytotoxicity, and anticancer activity of Spirulina maxima was investigated in this study. Optimal extraction conditions were determined as 60 kHz frequency at 60°C for 30 min with 120 W intensity, which resulted in 19.3% of extraction yields and 19.1% of cytotoxicity on normal human cells. Yields from conventional water and ethanol extraction were 15.8% at 100°C and 8.3% at 80°C, respectively. It was found that the extracts obtained by ultrasonic extraction process selectively inhibited the digestive-related cancer cell lines, such as human stomach cancer cells, having 89% of the highest inhibition ratio and 4.5 of the highest selectivity. In adding 0.5 mg/mL of the extract, human promyelocytic leukemia cells' cell differentiation was increased 1.72 times over that of the control. Expression level of B cell lymphoma-2 from Hep3B cell was also effectively suppressed by the extract obtained at 60 kHz and 60°C, leading to the inhibition of the early step of carcinogenesis. This work suggests that anticancer activity of the extracts is due to water-soluble polysaccharides rather than proteins and is further supported by the result that the ultrasonification extraction process can efficiently extract relatively intact polysaccharides rather than digesting the proteins in S. maxima by matrix assisted laser desorption ionization-time of flight and high performance size exclusion chromatography chromatogram analyses. Therefore, ultrasonic extraction increases both extraction yield and the biological activity of S. maxima extracts, which might be useful as an alternative natural anticancer agent in the medical and food industries.

Keywords

Spirulina maxima Ultrasonification low-temperature extraction Anticancer activity 

Notes

Acknowledgments

This work was supported by the Grant of the Korea Ministry of Education, Science and Technology (The Regional Core Research Program/Medical & Bio-Materials Research Consortium). Authors deeply appreciate their financial supports.

References

  1. Ahmed N, Weidemann MJ (1995) Biochemical effect of three different inhibitors of purine/pyrimidine metabolism on differentiation in HL60 cells. Leukemia Res 19:263–273CrossRefGoogle Scholar
  2. Bao Y, Yueming J, Mouming Z, John S, Lingzhao W (2008) Effects of ultrasonic extraction on the physical and chemical properties of polysaccharide from longan fruit pericarp. Polym Degrad Stab 93:268–272CrossRefGoogle Scholar
  3. Benito A, Grillot D, Nunez G, Fernandez-Luna J (1995) Regulation and function of Bcl-2 during differentiation-induced cell death in HL-60 promyelocytic cells. Am J Pathol 146:481–490PubMedGoogle Scholar
  4. Chen Y, Donghwa C, You SG (2008) Determination of physicochemical properties of sulphated fucans from sporophyll of Undaria pinnatifida using light scattering technique. Food Chem 111:503–507CrossRefGoogle Scholar
  5. Cho JH, Lee KM, Kim NS, Kang WH (1997) The effects of whitening components on human melanocytes in vitro. J Soc Cosmetic Sci Kor 23:115–121Google Scholar
  6. Doll R, Peto R (1981) The causes of cancer, quantitative estimates of avoidable risks of cancer in the United States today. J Natl Cancer Inst 66:1191–1308PubMedGoogle Scholar
  7. Doyle BT, O’Neill AJ, Fitzpatrick JM, Watson RWG (2004) Differentiation-induced HL-60 cell apoptosis: a mechanism independent of mitochondrial disruption? Apoptosis 9:345–352PubMedCrossRefGoogle Scholar
  8. Femenia A, Garcia-Mar M, Simal S, Rossell C, Blasco M (2001) Effects of supercritical carbon dioxide (SC-CO2) oil extraction on the cell wall composition of almond fruits. J Agric Food Chem 49:5828–5834PubMedCrossRefGoogle Scholar
  9. Grinstead GS, Tokach S, Goodband RD, Nelssen JL (2000) Effects of Spirulina platensis on growth performance of weanling pigs. Anim Feed Sci Technol 83:237–247CrossRefGoogle Scholar
  10. Ha JH, Han JG, Jeong HS, Oh SH, Kwon MC, Choi YB, Ko JR, Lee HY (2008) Enhancement of immune activities of natural water-soluble sulforaphane by nano encapsulation process. Korean J Medicinal Crop Sci 16:402–408Google Scholar
  11. Haldar S, Negrini M, Monne M, Sabbioni S, Croce CM (1994) Down-regulation of bcl-2 by p53 in breast cancer cells. Cancer Res 54:2095–2097PubMedGoogle Scholar
  12. Hamburger M, Baumann D, Adler S (2004) Supercritical carbon dioxide extraction of selected medical plants—effects of high pressure and added ethanol on yield of extracted substances. Phytochem Anal 15:46–54PubMedCrossRefGoogle Scholar
  13. Hernandez AC, Nieves I, Meckes M, Chamorro G, Barron B (2002) Antiviral activity of Spirulina maxima against herpes simplex virus type 2. Antiviral Res 56:279–285CrossRefGoogle Scholar
  14. Hwang CS, Choi JO, Kim IS (1995) Detection of bcl-2 & bax expression in the head & neck cancers. Cancer Res Treat 27:570–577Google Scholar
  15. Jeong SW, Lee NK, Kim SJ, Han DS (1995) Screening of tyrosinase inhibitor from plants. Korean J Food Sci Technol 27:891–896Google Scholar
  16. Jeong HS, Han JG, Ha JH, Kim Y, Oh SH, Kim SS, Jeong MH, Choi GP, Park UY, Lee HY (2009) Antioxidant activities and skin-whitening effects of nano-encapsuled water extract from Rubus coreanus Miquel. Korean J Medicinal Crop Sci 17:83–89Google Scholar
  17. Kang CM, Lee HY, Kim SI (1998) Effects of triterpene acids and ginsenosides on differentiation of HL-60 promyelocytic leukemia cells. Korean J Life Sci 8:162–166Google Scholar
  18. Kaufmann B, Christen P (2002) Recent extraction techniques for natural products: microwave-assisted extraction and pressurised solvent extraction. Phytochem Anal 13:105–113PubMedCrossRefGoogle Scholar
  19. Kay RA (1991) Microalgae as food and supplement. Crit Rev Food Sci Nutr 30:555–573PubMedCrossRefGoogle Scholar
  20. Kim IS, Jo JS (1993) Modulation of human fibroblast proliferation and collagen production by prostaglandin E2: association of intracelluar cyclic AMP and changes in prostaglandin E2 responsiveness. Korean Biochem J 26:40–52Google Scholar
  21. Kim US, Lee KJ (2009) Extraction of genistein and formononetin from Sophora flavescens Aiton using ultrasonic wave. Korean Chem Eng Res 47:258–261Google Scholar
  22. Kim HS, Kim CH, Kim JH, Kwon MC, Cho JH, Gwak HG, Hwang BY, Kim JC, Lee HY (2006a) Comparison of anticancer activities from the culture and extraction conditions of the Spirulina platensis. Korean J Microbiol Biotechnol 34:143–149Google Scholar
  23. Kim HS, Kim CH, Kwon MC, Song YK, Cho JH, Gwak HG, Hwang BY, Kim JC, Lee HY (2006b) Anticancer activity of ultrasonified extracts from seawater-based culture of the microalga Spirulina platensis. J Korean Fish Soc 39:318–325Google Scholar
  24. Langdon SP, Hickman JA (1987) Correlation between the molecular weight and potency of polar compounds which induce the differentiation of HL-60 human promyelocytic leukemia cells. Cancer Res 47:140–144PubMedGoogle Scholar
  25. Lee TJ, Lee JS, Choi JE, Bae JJ, Lee TY (2002) The effect of mycolactone on the expression of Bcl-2 family genes in Hep3B hepatoma cells. J Bacteriol Virol 32:55–61Google Scholar
  26. Lee JJ, Shin DH, Park SE, Kim WI, Park DI, Choi YH, Hong SH (2008) Euphorbiae humifusae sensitizes apoptosis of TRAIL-resistant human gastric adenocarcinoma AGS cells. J Life Sci 18:120–128Google Scholar
  27. Nandeesha MC, Gangadhara B, Manissery JK, Venkataraman LV (2001) Growth performance of two Indian major carps, catla (Catla catla) and rohu (Labeo rohita) fed diets containing different levels of Spirulina platensis. Bioresource Technol 80:117–120CrossRefGoogle Scholar
  28. Oh SH, Han JG, Ha JH, Kim Y, Jeong MH, Kim SS, Jeong HS, Choi GP, Park UY, Kang DH, Lee HY (2009) Enhancement of immune activity of Spirulina maxima by low temperature ultrasonification extraction. Korean J Food Sci Technol 41:313–319Google Scholar
  29. Qadir SA, Kwon MC, Han JG, Ha JH, Chung HS, Ahn J, Lee HY (2009) Effect of different extraction protocols on anticancer and antioxidant activities of Berberis koreana bark extracts. J Biosci Bioeng 107:331–338PubMedCrossRefGoogle Scholar
  30. Reed JC (1994) Bcl-2 and the regulation of programmed cell death. J Cell Biol 124:1–6PubMedCrossRefGoogle Scholar
  31. Reed TJ, Miyashita T, Takayama S (1996) Bcl-2 family proteins: regulators of cell death involved in the pathogenesis of cancer and resistance to therapy. J Cell Biochem 60:23–32PubMedCrossRefGoogle Scholar
  32. Seo JH, Rah JC, Choi SH, Shin JK, Min K, Kim HS, Park CH, Kim S, Kim EM, Lee SH, Lee S, Suh SW, Suh YH (2002) a-Synuclein regulates neuronal survival via Bcl-2 family expression and PI3/Akt kinase pathway. FASEB J 16:1826–1828PubMedGoogle Scholar
  33. Sharma UK, Sharma K, Sharma N, Sharma A, Singh HP, Sinha AK (2008) Microwave-assisted efficient extraction of different parts of Hippophae rhamnoides for the comparative evaluation of antioxidant activity and quantification of its phenolic constituents by reverse-phase high-performance liquid chromatography (RP-HPLC). J Agric Food Chem 56:374–379PubMedCrossRefGoogle Scholar
  34. Shrestha RP, Weinstein Y, Bar-Zvi D, Arad SA (2004) Glycoprotein noncovalently associated with cell-wall polysaccharide of the red microalga Porphyridium sp. (Rhodophyta). J Phycol 40:568–580CrossRefGoogle Scholar
  35. Stegh AH, Barnhart BC, Volkland J, Algeciras SA, Ke N, Reed JC, Peter ME (2002) Inactivation of caspase-8 on mitochondria of Bcl-xL-expressing MCF-7-Fas cells. Role for the bifunctional apoptosis regulator protein. J Biol Chem 277:4351–4360PubMedCrossRefGoogle Scholar
  36. Thomas WD, Hersey P (1998) TNF-related apoptosis-inducing ligand (TRAIL) induces apoptosis in Fas ligand-resistant melanoma cells and mediates CD4 T cell killing of target cells. J Immunol 161:2195–2200PubMedGoogle Scholar
  37. Yang HN, Lee EH, Kim HM (1997) Spirulina platensis inhibits anaphylactic reaction. Life Sci 61:1237–1244PubMedCrossRefGoogle Scholar
  38. Yen A, Guernsey DL (1986) Increased c-myc RNA levels associated with the precommitment state during HL-60 myeloid differentiation. Cancer Res 46:4156–4161PubMedGoogle Scholar
  39. Youn CK, Cho HJ, Kim SH, Kim HB, Kim MH, Chang IY, Lee JS, Chung MH, Hahm KS, You HJ (2005) Bcl-2 expression suppresses mismatch repair activity through inhibition of E2F transcriptional activity. Nat Cell Biol 7:137–147PubMedCrossRefGoogle Scholar
  40. Zhang S, Zhang J, Wang C (2007) Extraction of steroid saponins from Paris polyphylla Sm. var. yunnanensis using novel ultrahigh pressure extraction technology. Pharmaceut Chem J 41:424–429CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Sung-Ho Oh
    • 1
  • Juhee Ahn
    • 1
  • Do-Hyung Kang
    • 2
  • Hyeon-Yong Lee
    • 1
    • 3
  1. 1.College of Bioscience and Biotechnology Division of Biomaterials EngineeringKangwon National UniversityChuncheonSouth Korea
  2. 2.Korea Ocean Research & Development InstituteSeoulSouth Korea
  3. 3.Research Institute of Bioscience and BiotechnologyKangwon National UniversityChuncheonSouth Korea

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