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Extract of Saccharina japonica Induces Apoptosis companied by Cell Cycle Arrest and Endoplasmic Reticulum Stress in SK-Hep1 Human Hepatocellular Carcinoma Cells

  • Jung, Hyun Il (Department of Microbiology, College of Natural Sciences, Pukyong National University) ;
  • Jo, Mi Jeong (Department of Microbiology, College of Natural Sciences, Pukyong National University) ;
  • Kim, Hyung-Rak (Department of Food Science and Nutrition, College of Fishery Sciences, Pukyong National University) ;
  • Choi, Yung Hyun (Department of Biochemistry, College of Oriental Medicine, Dongeui University) ;
  • Kim, Gun-Do (Department of Microbiology, College of Natural Sciences, Pukyong National University)
  • Published : 2014.04.01

Abstract

Saccharina japonica is a family member of Phaeophyceae (brown macro-alga) and extensively cultivated in China, Japan and Korea. Here, the potential anti-cancer effect of n-hexane fraction of S. japonica was evaluated in SK-Hep1 human hepatocellular carcinoma cells. The N-hexane fraction reduced cell viability and increased the numbers of apoptotic cells in a both dose- and time-dependent manner. Apoptosis was activated by both caspase-dependent and independent pathways. The caspase-dependent cell death pathway is mediated by cell surface death receptors and activated caspase-8 amplified the apoptotic signal either through direct activation of downstream caspase-3 or pro-apoptotic proteins (Bad, Bax and Bak) subsequently leading to the release of cytochrome c. On the other hand, caspase-independent apoptosis appeared mediated by disruption of mitochondrial membrane potential and translocation of AIF to the nucleus where they induced chromatin condensation and/or large-scale DNA fragmentation. In addition, the n-hexane fraction induced endoplasmic reticulum (ER)-stress and cell cycle arrest. The results suggested that potential anti-cancer effects of n-hexane extract from S. japonica on SK-Hep1 cells.

Keywords

Caspase-dependent/independent apoptosis;Hep1 cells;cell cycle arrest;ER-stress;Saccharina japonica

Acknowledgement

Supported by : Pukyong National University

References

  1. Rebecca S, Deepa N, Ahmedin J (2013). Cancer statistics, 2013. CA Cancer J Clin, 63, 11-30. https://doi.org/10.3322/caac.21166
  2. Ohigashi H, Sakai Y, Yamaguchi K, et al (1992). Possible anti-tumor promoting properties of marine algae and in vivo activity of Wakame seaweed extract. Biosci Biotech Biochem, 56, 994-5. https://doi.org/10.1271/bbb.56.994
  3. Oyadomari S, Araki E, Mori M (2002). Endoplasmic reticulum stress-mediated apoptosis in pancreatic ${\beta}$-cells. Apoptosis, 7, 335-45. https://doi.org/10.1023/A:1016175429877
  4. Plouguerne E, de Souza LM, Sassaki GL,et al (2013). Antiviral Sulfoquinovosyldiacylglycerols (SQDGs) from the Brazilian brown seaweed Sargassum vulgare. Mar Drugs, 11, 4628-40. https://doi.org/10.3390/md11114628
  5. Senthilkumar K, Manivasagan P, Venkatesan J, et al (2013). Brown seaweed fucoidan: biological activity and apoptosis, growth signaling mechanism in cancer. Int J Biol Macromol, 60, 366-74. https://doi.org/10.1016/j.ijbiomac.2013.06.030
  6. Sevrioukova IF (2011). Apoptosis-inducing factor: structure, function, and redox regulation. Antioxid Redox Signal, 14, 2545-79. https://doi.org/10.1089/ars.2010.3445
  7. Voeltz GK, Rolls MM, Rapoport TA (2002). Structural organization of the endoplasmic reticulum. EMBO Rep, 3, 944-50. https://doi.org/10.1093/embo-reports/kvf202
  8. Wang WA, Groenendyk J, Michalak M (2014). Endoplasmic reticulum stress associated responses in cancer. Biochim Biophys Acta, [Epub ahead of print].
  9. Wurstle ML, Laussmann MA, Rehm M (2012). The central role of initiator caspase-9 in apoptosis signal transduction and the regulation of its activation and activity on the apoptosome. Exp Cell Res, 318, 1213-20. https://doi.org/10.1016/j.yexcr.2012.02.013
  10. Zhao YJ, Wang JH, Fu B, et al (2009). Effects of 3-aminobenzamide on expressions of poly (ADP ribose) polymerase and apoptosis inducing factor in cardiomyocytes of rats with acute myocardial infarction. Chin Med J, 122, 1322-7.
  11. Kaufman RJ (1999). Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev, 13, 1211-3. https://doi.org/10.1101/gad.13.10.1211
  12. Jacobson MD, Weil M, Raff MC (1997). Programmed cell death in animal development. Cell, 88, 347-54. https://doi.org/10.1016/S0092-8674(00)81873-5
  13. Jin Z, El-Deiry WS (2005). Overview of cell death signaling pathways. Cancer Biol Ther, 4, 139-63.
  14. Jo MJ, Kim HR, Kim G-D (2012). The anticancer effects of Saccharina japonica on 267B1/K-ras human prostate cancer cells. Int J Oncol, 41, 1789-97. https://doi.org/10.3892/ijo.2012.1612
  15. Khan KH, Blanco-Codesido M, Molife LR (2013). Cancer therapeutics: Targeting the apoptotic pathway. Crit Rev Oncol Hematol, 13, 267-9.
  16. Kim J, Jayaprakasha GK, Vikram A, et al (2012). Methyl nomilinate from citrus can modulate cell cycle regulators to induce cytotoxicity in human colon cancer (SW480) cells in vitro. Toxicol in vitro, 26, 1216-23. https://doi.org/10.1016/j.tiv.2012.06.005
  17. Li XC, Jacob MR, Ding Y, et al (2006). Capisterones A and B, which enhance fluconazole activity in Saccharomyces cerevisiae, from the marine green alga Penicillus capitatus. J Nat Prod, 69, 542-6. https://doi.org/10.1021/np050396y
  18. Manivannan K, Karthikai Devi G, Anantharaman P, et al (2011). Antimicrobial potential of selected brown seaweeds from Vedalai coastal waters, Gulf of Mannar. Asian Pac J Trop Biomed, 1, 114-20. https://doi.org/10.1016/S2221-1691(11)60007-5
  19. Matsuhiro B, Conte AF, Damonte EB, et al (2005). Structural analysis and antiviral activity of a sulfated galactan from the red seaweed Schizymenia binderi (Gigartinales, Rhodophyta). Carbohydr Res, 340, 2392-402. https://doi.org/10.1016/j.carres.2005.08.004
  20. Muthuirulappan S, Francis SP (2013). Anti-cancer mechanism and possibility of nano-suspension formulations for a marine algae product fucoxanthin. Asian Pac J Cancer Prev, 14, 2213-6. https://doi.org/10.7314/APJCP.2013.14.4.2213
  21. Boland ML, Chourasia AH, Macleod KF (2013). Mitochondrial dysfunction in Cancer. Front Oncol, 3, 292.
  22. Ahn HK, Lee S, Sun JM, et al (2011). Sequential therapy with sunitinib and sorafenib in metastatic hepatocellular carcinoma. Invest New Drugs, 30, 1768-72.
  23. Allan LA, Clarke PR (2009). Apoptosis and autophagy: Regulation of caspase-9 by phosphorylation. FEBS J, 276, 6063-73. https://doi.org/10.1111/j.1742-4658.2009.07330.x
  24. Ashkenazi A, Dixit VM (1998). Death receptors: signaling and modulation. Science, 281, 1305-8. https://doi.org/10.1126/science.281.5381.1305
  25. Bossy-Wetzel E, Newmeyer DD, Green DR (1998). Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J, 17, 37-49. https://doi.org/10.1093/emboj/17.1.37
  26. Cregan SP, Dawson VL, Slack RS (2004). Role of AIF in caspase-dependent and caspase-independent cell death. Oncogene, 23, 2785-96. https://doi.org/10.1038/sj.onc.1207517
  27. Donnelly N, Gorman AM, Gupta S, et al (2013). The $eIF2{\alpha}$ kinases: their structures and functions. Cell Mol Life Sci, 70, 3493-11. https://doi.org/10.1007/s00018-012-1252-6
  28. Fitton JH (2003). Brown marine algae: a survey of therapeutic potentials. Altern Complement Ther, 9, 29-33. https://doi.org/10.1089/10762800360520767
  29. Funahashi H, Imai T, Tanaka Y, et al (1999). Wakame seaweed suppresses the proliferation of 7, 12-dimethylbenz (a)-anthracene-induced mammary tumors in rats. Cancer Sci, 90, 922-7. https://doi.org/10.1111/j.1349-7006.1999.tb00836.x
  30. Hu Q, Wu D, Chen W, et al (2013). Proteolytic processing of the caspase-9 zymogen is required for apoptosome-mediated activation of caspase-9. J Biol Chem, 288, 15142-7. https://doi.org/10.1074/jbc.M112.441568
  31. Itoh H, Noda H, Amano H, et al (1995). Immunological analysis of inhibition of lung metastases by fucoidan (GIV-A) prepared from brown seaweed Sargassum thunbergii. Anticancer Res, 15, 1937-47.

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