Food Science and Biotechnology

Korean Society of Food Science and Technology (한국식품과학회)
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Antitumor Activities of Sea Staghorn (Codium fragile) against CT-26 Cells

  • Kim, Kil-Nam (Faculty of Applied Marine Science, Cheju National University) ;
  • Kim, Soo-Hyun (Faculty of Food Science Engineering, Cheju National University) ;
  • Kim, Won-Suk (Binex Co., Ltd.) ;
  • Kang, Sung-Myung (Faculty of Applied Marine Science, Cheju National University) ;
  • Lee, Ki-Wan (Faculty of Applied Marine Science, Cheju National University) ;
  • Lee, Wook-Jae (Jeju Biodiversity Research Institute, Jeju Hi-Tech Industry Development Institute) ;
  • Park, Soo-Yeong (Jeju Biodiversity Research Institute, Jeju Hi-Tech Industry Development Institute) ;
  • Kim, Se-Kwon (Department of Chemistry, Pukyong National University) ;
  • Jeon, You-Jin (Faculty of Applied Marine Science, Cheju National University)
  • Published : 2008.10.31
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Abstract

The 10 species of marine green algae was collected from Jejudo(Island) in Korea. Methanolic and aqueous extracts were prepared and screened for inhibition activities against tumor cell growth. Of the tested samples, the sea staghorn (Codium fragile) aqueous extract (CFAE) showed the highest activity on CT-26 cell growth. Therefore, CFAE was selected for further experiments and the possibility to induce apoptosis by the CFAE was investigated. Flow cytometric analysis revealed that it dose-dependently increased apoptotic cells with hypodiploid DNA contents in CT-26 cell line. These results indicated that CFAE can suppress the growth of CT-26 cells through apoptosis. The CFAE decreased the protein expression of anti-apoptotic Bcl-xL and led to the activation of caspase-3 and -7. A crude polysaccharide was separated from CFAE and it mainly constituted with 61.2% galactose and 30.5% arabinose as analyzed by high performance liquid chromatography (HPLC).

Keywords

References

  1. Ferguson LR, Philpott M, Karunasinghe N. Dietary cancer and prevention using antimutagens. Toxicology 198: 147-159 (2004) https://doi.org/10.1016/j.tox.2004.01.035
  2. Satia-Abouta J, Galanko JA, Martin CF, Ammerman A, Sandler RS. Food groups and colon cancer risk in African-Americans and Caucasians. Int. J. Cancer 109: 728-736 (2004) https://doi.org/10.1002/ijc.20044
  3. O'Connell JB, Maggard MA, Liu JH, Etzioni DA, Livingston EH, Ko CY. Rates of colon and rectal cancers are increasing in young adults. Am. Surgeon 69: 866-872 (2003)
  4. Wils J. Adjuvant treatment of colon cancer: Past, present, and future. J. Chemother. 19: 115-122 (2007) https://doi.org/10.1179/joc.2007.19.2.115
  5. Howard CV, Newby JA. Could the increase in cancer incidence be related to recent environmental changes. pp. 39-56. In: Cancer as An Environmental Disease. NicolopoulouStamati P, Hens L, Howard CV, VanLarebeke N (eds). Kluwer Academic Publishers, Dordrecht, Netherlands (2004)
  6. Szelenyi H, Hohenberger P, Lochs H, Haboubi N, Berdel WE, Thiel E, Kreuser ED. Sequential trimetrexate, 5-fluorouracil, and folinic acid are effective and well tolerated in metastatic colorectal carcinoma. Oncology 58: 273-279 (2000) https://doi.org/10.1159/000012112
  7. Clark JW. Perspectives on new chemotherapeutic agents in the treatment of colorectal cancer. Semin. Oncol. 24: 19-24 (1997)
  8. von Hoff DD. Promising new agents for treatment of patients with colorectal cancer. Semin. Oncol. 25: 47-52 (1998)
  9. Shinkai K, Akedo H, Mukai M, Imamura F, Isoai A, Kobayashi M, Kitagawa I. Inhibition of in vitro tumor cell invasion by ginsenoside $Rg_3$. Jpn. J. Cancer Res. 87: 357-362 (1996) https://doi.org/10.1111/j.1349-7006.1996.tb00230.x
  10. Ahmad N, Feyes DK, Nieminen AL, Agarwal R, Mukhtar H. Green tea constituent epigallocatechin-3-gallate and induction of apoptosis and cell cycle arrest in human carcinoma cells. J. Natl. Cancer I. 89: 1881-1886 (1997) https://doi.org/10.1093/jnci/89.24.1881
  11. Kim YS, Jin SH, Lee YH, Kim SI, Park JD. Ginsenoside Rh2 induces apoptosis independently of Bcl-2 Bcl-xL, or Bax in C6Bu-1 cells. Arch. Pharm. Res. 22: 448-453 (1999) https://doi.org/10.1007/BF02979151
  12. Zhu W, Chiu LCM, Ooi VEC, Chan PKS, Ang PO. Antiviral property and mechanisms of a sulphated polysaccharide from the brown alga Sargassum patens against Herpes simplex virus type 1. Phytomedicine 13: 695-701 (2006) https://doi.org/10.1016/j.phymed.2005.11.003
  13. Oh KB, Lee JH, Chung SC, Shin J, Shin HJ, Kim HK, Lee HS. Antimicrobial activities of the bromophenols from the red alga Odonthalia corymbifera and some synthetic derivatives. Bioorgan. Med. Chem. Lett. 18: 104-108 (2008) https://doi.org/10.1016/j.bmcl.2007.11.003
  14. Bennamara A, Abourriche A, Berrada M, Charrouf M, Chaib N, Boudouma M, Garneau FX. Methoxybifurcarenone: An antifungal and antibacterial meroditerpenoid from the brown alga Cystoseira tamariscifolia. Phytochemistry 52: 37-40 (1999) https://doi.org/10.1016/S0031-9422(99)00040-0
  15. Glombitza KW, Koch M. Secondary metabolites of pharmaceutical potential. pp. 161-238. In: Algal and Cyanobacterial Biotechnology. Cresswell RC, Rees TAV, Shah N (eds). Longman Scientific & Technical, Harlow, Essex, England (1989)
  16. Kwon HJ, Bae SY, Kim KH, Han CH, Cho SH, Nam SW, Choi YH, Kim BW. Induction of apoptosis in HeLa cells by ethanolic extract of Corallina pilulifera. Food Chem. 104: 196-201 (2007) https://doi.org/10.1016/j.foodchem.2006.11.031
  17. Cavas L, Baskin Y, Yurdakoc K, Olgun N. Antiproliferative and newly attributed apoptotic activities from an invasive marine alga: Caulerpa racemosa var. cylindracea. J. Exp. Mar. Biol. Ecol. 339: 111-119 (2006) https://doi.org/10.1016/j.jembe.2006.07.019
  18. Athukorala Y, Kim KN, Jeon YJ. Antiproliferative and antioxidant properties of an enzymatic hydrolysate from brown alga, Ecklonia cava. Food Chem. Toxicol. 44: 1065-1074 (2006) https://doi.org/10.1016/j.fct.2006.01.011
  19. Zhou G, Xin H, Sheng W, Sun Y, Li Z, Xu Z. In vivo growthinhibition of S180 tumor by mixture of 5-Fu and low molecular ${\gamma}-carrageenan$ from Chondrus ocellatus. Pharmacol. Res. 51: 153-157 (2005) https://doi.org/10.1016/j.phrs.2004.07.003
  20. Zhang YS. Dictionary of Chinese Marine Drugs. China Ocean Press, Beijing, China. p. 507 (1994)
  21. Gschwind M, Huber G. Apoptotic cell death induced by ${\beta}-amyloid$ 1-42 peptide is cell type dependent. J. Neurochem. 65: 292-300 (1995) https://doi.org/10.1046/j.1471-4159.1995.65010292.x
  22. Lizard G, Fournel S, Genestier L, Dhedin N, Chaput C, Flacher M, Mutin M, Panaye G, Revillard JP. Kinetics of plasma membrane and mitochondrial alterations in the cells undergoing apoptosis. Cytometry 21: 275-283 (1995) https://doi.org/10.1002/cyto.990210308
  23. Nicoletti I, Migliorati G, Pagliacci MC, Grignani F, Riccardi C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 139: 271-279 (1991) https://doi.org/10.1016/0022-1759(91)90198-O
  24. Wang XW, Zhan Q, Coursen JD, Khan MA, Kontny HU, Yu L, Hollander MC, O'Connor PM, Fornace AJ, Harris CC. GADD45 induction of a $G_2/M$ cell cycle checkpoint. P. Natl. Acad. Sci. USA 96: 3706-3711 (1999)
  25. Matsubara K, Matsuura Y, Hori K, Miyazawa K. An anticoagulant proteoglycan from the marine green alga, Codium pugniformis. J. Appl. Phycol. 12: 9-14 (2000) https://doi.org/10.1023/A:1008174115350
  26. Kuda T, Taniguchi E, Nishizawa M, Araki Y. Fate of water-soluble polysaccharides in dried Chorda filum, a brown alga during water washing. J. Food Compos. Anal. 15: 3-9 (2002) https://doi.org/10.1006/jfca.2001.1037
  27. Staub AM. Removeal of protein-Sevag method. Methods Carbohyd. Chem. 5: 5-6 (1965)
  28. Harada H, Kamei Y. Selective cytotoxicity of marine algae extracts to several human leukemic cell lines. Cytotechnology 25: 213-219 (1997) https://doi.org/10.1023/A:1007987010840
  29. Nara T, Kamei Y, Tsubouchi A, Annoura T, Hirota K, Iizumi K, Dohmoto Y, Ono T, Aoki T. Inhibitory action of marine algae extracts on the Trypanosoma cruzi dihydroorotate dehydrogenase activity and on the protozoan growth in mammalian cells. Parasitol. Int. 54: 59-64 (2005) https://doi.org/10.1016/j.parint.2004.11.001
  30. Kwon MJ, Nam TJ. Chromatographically purified porphyran from Porphyra yezoensis effectively inhibits proliferation of human cancer cells. Food Sci. Biotechnol. 16: 873-878 (2007)
  31. Noda H, Amano H, Arashima K, Hashimoto S, Nisizawa K. Antitumor activity of marine algae. Hydrobiologia 204/205: 577-584 (1990) https://doi.org/10.1007/BF00040290
  32. Chi HY, Lee CH, Kim KH, Kim SL, Chung IM. Induction of apoptosis cell death by red pericarp rice ('Jakwangchalbyeo') extracts. Food Sci. Biotechnol. 15: 534-542 (2006)
  33. Cha MR, Kim JY, Hwang JH, Park HR. Induction of cytotoxicity and apoptosis in HT-29 human colon carcinoma cells by a Gleditsiae Semen extract. Food Sci. Biotechnol. 16: 260-264 (2007)
  34. Hengartner MO. The biochemistry of apoptosis. Nature 407: 770-776 (2000) https://doi.org/10.1038/35037710
  35. Kaufmann S, Hengartner MO. Programmed cell death: Alive and well in the new millennium. Trends Genet. 11: 526-534 (2001)
  36. Bold RJ, Termuhlen PM, McConkey DJ. Apoptosis, cancer, and cancer therapy. Surg. Oncol. 6: 133-142 (1997) https://doi.org/10.1016/S0960-7404(97)00015-7
  37. Hu W, Kavanagh JJ. Anticancer therapy targeting the apoptotic pathway. Lancet Oncol. 4: 721-729 (2003) https://doi.org/10.1016/S1470-2045(03)01277-4
  38. Buttke TM, Sandstrom PA. Oxidative stress as a mediator of apoptosis. Immunol. Today 15: 7-10 (1994) https://doi.org/10.1016/0167-5699(94)90018-3
  39. Wyllie AH. The biology of cell death in tumor. Anticancer Res. 5: 131-142 (1985) https://doi.org/10.1097/00001813-199404000-00002
  40. Korsmeyer SJ. Bcl-2 gene family and the regulation of programmed cell death. Cancer Res. 59: 1693-1700 (1999)
  41. Hockenbery DM, Oltvai ZN, Yin XM, Milliman CL, Korsmeyer SJ. Bcl-2 function in an antioxidant pathway to prevent apoptosis. Cell 75: 241-251 (1993) https://doi.org/10.1016/0092-8674(93)80066-N
  42. Fernandes-Alnemri T, Litwack G, Alnemri ES. CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein Ced-3 and mammalian interleukin-1 betaconverting enzyme. J. Biol. Chem. 269: 30761-30764 (1994)
  43. Fernandes-Alnemri T, Takahashi A, Armstrong R, Krebs J, Fritz L, Tomaselli KJ, Wang L, Yu Z, Croce CM, Salveson G. Mch3, a novel human apoptotic cysteine protease highly related to CPP32. Cancer Res. 55: 6045-6052 (1995)
  44. Duan H, Chinnaiyan AM, Hudson PL, Wing JP, He WW, Dixit VM. ICE-LAP3, a novel mammalian homologue of the Caenorhabditis elegans cell death protein Ced-3 is activated during Fas- and tumor necrosis factor-induced apoptosis. J. Biol. Chem. 271: 1621-1625 (1996) https://doi.org/10.1074/jbc.271.3.1621
  45. Lippke JA, Gu Y, Sarnecki C, Caron PR, Su MS. Identification and characterization of CPP32/Mch2 homolog 1, a novel cysteine protease similar to CPP32. J. Biol. Chem. 271: 1825-1828 (1996) https://doi.org/10.1074/jbc.271.4.1825
  46. Cohen JJ, Duke RC, Fadok VA, Sellins KS. Apoptosis and programmed cell death in immunity. Annu. Rev. Immunol. 10: 267-293 (1992) https://doi.org/10.1146/annurev.iy.10.040192.001411
  47. Nunez G, Benedict MA, Hu Y, Inohara N. Caspases: The proteases of the apoptotic pathway (review). Oncogene 17: 3237-3245 (1998) https://doi.org/10.1038/sj.onc.1202581
  48. Frantz G. Polysaccharides in pharmacy: Current applications and future concepts. Planta Med. 55: 493-497 (1989) https://doi.org/10.1055/s-2006-962078
  49. DePhilippis R, Vincenzini M. Exocellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiol. Rev. 22: 151-175 (1998) https://doi.org/10.1111/j.1574-6976.1998.tb00365.x
  50. Guven KC, Ozsoy Y, Ulutin ON. Anticoagulant, fibrinolytic, and antiaggregant activity of carrageenans and alginic acid. Bot. Mar. 34: 429-432 (1991) https://doi.org/10.1515/botm.1991.34.5.429
  51. Zhang Q, Li N, Zhou G, Lu X, Xu Z, Li Z. In vivo antioxidant activity of polysaccharide fraction from Porphyra haitanesis (Rhodephyta) in aging mice. Pharmacol. Res. 48: 151-155 (2003) https://doi.org/10.1016/S1043-6618(03)00103-8
  52. Love J, Percival E. The polysaccharides of the green seaweed Codium fragile. Part III. A ${\beta}-1,4-linked$ mannan. J. Chem. Soc. 3345-3350 (1964) https://doi.org/10.1039/jr9640003345
  53. Ciancia M, Quintana I, Vizcarguenaga MI, Kasulin L, de Dios A, Estevez JM, Cerezo AS. Polysaccharides from the green seaweeds Codium fragile and C. Vermilara with controversial effects on hemostasis. Int. J. Biol. Macromol. 41: 641-649 (2007) https://doi.org/10.1016/j.ijbiomac.2007.08.007
  54. Ruperez P, Ahrazem O, Leal JA. Potential antioxidant capacity of sulfated polysaccharides from the edible marine brown seaweed Fucus vesiculosus. J. Agr. Food Chem. 50: 840-845 (2002) https://doi.org/10.1021/jf010908o
  55. Umemura K, Yanase K, Suzuki M, Okutani K, Yamori T, Andoh T. Inhibition of DNA topoisomerases I and II, and growth inhibition of human cancer cell lines by a marine microalgal polysaccharide. Biochem. Pharmacol. 66: 481-487 (2003) https://doi.org/10.1016/S0006-2952(03)00281-8
  56. Zhou G, Sun YP, Xin H, Zhang Y, Li Z, Xu Z. In vivo antitumor and immunomodulation activities of different molecular weight lambdacarrageenans from Chondrus ocellatus. Pharmacol. Res. 50: 47-53 (2004) https://doi.org/10.1016/j.phrs.2003.12.002