DOI QR코드

DOI QR Code

Red Sea Cucumber (Stichopus japonicus) Suppresses Cancer Progression by Promoting the ROS-Me diated Inhibition of the MAPK Pathway

  • Kim, Jusnseong (Jeju Marine Research Center, Korea Institute of Ocean Science and Technology (KIOST)) ;
  • Kim, Eun-A (Jeju Marine Research Center, Korea Institute of Ocean Science and Technology (KIOST)) ;
  • Kang, Nalae (Jeju Marine Research Center, Korea Institute of Ocean Science and Technology (KIOST)) ;
  • Choi, Youn Kyung (Department of Medicine, School of Medicine, Jeju National University) ;
  • Heo, Soo-Jin (Jeju Marine Research Center, Korea Institute of Ocean Science and Technology (KIOST))
  • Received : 2020.07.03
  • Accepted : 2020.12.24
  • Published : 2020.12.31

Abstract

Stichopus japonicas (red sea cucumbers) inhabit the coastal sea surrounding Jeju Island, South Korea, and are thought to have various medicinal properties. In this study, we investigated the anticancer activity of a red sea cucumber (S. japonicus) collected from Jeju Island. We obtained the red sea cucumber extract (RSCE), and observed that it inhibited the tumor cell growth and increased reactive oxygen species (ROS) production associated with the induction of apoptosis through the mitogen-activated protein kinase (MAPK) pathway in murine colon carcinoma cells (CT-26). Treatment with RSCE and N-acetylcysteine, which is a ROS scavenger, increased ROS production and apoptosis via the regulation by the MAPK pathway on the ERK and JNK compared with the nontreated group. Therefore, RSCE promotes ROS-mediated suppression of the ERK and JNK activation, and subsequently inhibits cancer progression, suggesting that RSCE may be beneficial in treating colon carcinoma.

Keywords

References

  1. Ahmedin Jemal, Freddile Bray, Melissa M Center, Jacques Ferlay, Elizabeth Ward and David Forman. 2011. Global cancer statistics. CA: a cancer journal for clinicians 61(2): 69-90. https://doi.org/10.3322/caac.20107
  2. Allal Ouhtit, Rajiv Lochan Gaur, Mohamed Abdraboh, Shubha K. Ireland, Prakash N Rao, Shailaja GRaj, Hamad Al-Riyami, Somya Shanmuganathan, Ishita Gupta, Subramanyam N Murthy, Andrew Hollenbach and Madhwa HG Raj. 2013. Simultaneous inhibition of cell-cycle, proliferation, survival, metastatic pathways and induction of apoptosis in breast cancer cells by a phytochemical super-cocktail: Genes that underpin its mode of action. Journal of Cancer 4(9): 703. https://doi.org/10.7150/jca.7235
  3. Atsushi Matsuzawa and Hidenori Ichijo. 2005. Stress-responsive protein kinases in redox-regulated apoptosis signaling. Antioxidants & redox signaling 7(3-4): 472-481. https://doi.org/10.1089/ars.2005.7.472
  4. Bobbili V.V. Pardhasaradhi, A. Mubarak Ali, A. Leela Kumari, Pallu Reddanna and Ashok Khar. 2003. Phycocyanin-mediated apoptosis in ak-5 tumor cells involves down-regulation of bcl-2 and generation of ros. Molecular cancer therapeutics 2(11): 1165-1170.
  5. Chong Sun and Rene Bernards. 2014. Feedback and redundancy in receptor tyrosine kinase signaling: Relevance to cancer therapies. Trends in biochemical sciences 39(10): 465-474. https://doi.org/10.1016/j.tibs.2014.08.010
  6. Coutney L. Robertson, Susanna Scafidi, Mary C. Mc Kenna and Gary Fiskum. 2009. Mitochondrial mechanisms of cell death and neuroprotection in pediatric ischemic and traumatic brain injury. Experimental neurology 218(2): 371-380. https://doi.org/10.1016/j.expneurol.2009.04.030
  7. Dennis J. Goussetis and Leonidas C. Platanias. 2010. Arsenic trioxide and the pi3k/akt pathway in chronic lymphocytic leukemia. Clinical Cancer Research: clincanres. 1496. subyr.
  8. Emile Tan, Henry Tilney, Mike Thompson, Jason Smith, Paris P. Tekkis and Britain AoCoG. 2007. The united kingdom national bowel cancer project-epidemiology and surgical risk in the elderly. European journal of cancer 43(15): 2285-2294. https://doi.org/10.1016/j.ejca.2007.06.009
  9. Fang Tian, Xiongwen Zhang, Yungyuang Tong, Yanghua Yi, Shilong Zhang, Ling Li, Peng Sun, Liping Lin and Jian Ding. 2005. Pe, a new sulfated saponin from sea cucumber, exhibits anti-angiogenic and anti-tumor activities in vitro and in vivo. Cancer biology & therapy 4(8): 874-882. https://doi.org/10.4161/cbt.4.8.1917
  10. Haider Raza, Annie John and Sheela Benedict. 2011. Acetylsalicylic acid-induced oxidative stress, cell cycle arrest, apoptosis and mitochondrial dysfunction in human hepatoma hepg2 cells. European journal of pharmacology 668(1-2): 15-24. https://doi.org/10.1016/j.ejphar.2011.06.016
  11. Hua Li Xu, Xiao Feng Yu, Shao Chun Qu, Xiang Ru Qu and Yan Fang Jiang. 2012. Juglone, from juglans mandshruica maxim, inhibits growth and induces apoptosis in human leukemia cell hl-60 through a reactive oxygen species-dependent mechanism. Food and chemical toxicology 50(3-4): 590-596. https://doi.org/10.1016/j.fct.2012.01.002
  12. Irina Vasilevskaya and Peter J. O'Dwyer. 2003. Role of jun and jun kinase in resistance of cancer cells to therapy. Drug resistance updates 6(3): 147-156. https://doi.org/10.1016/S1368-7646(03)00043-8
  13. Jin Hyang Yang. 2005. The effect of foot reflexolog y on nausea, vomiting and fatigue of breast cancer patients undergoing chemotherapy. Journal of Korean Academy of Nursing 35(1): 177-185. https://doi.org/10.4040/jkan.2005.35.1.177
  14. Jung-Ha Kang, Ki-Hwan Yu, Jung-Youn Park, Chul-Min An, Je-Cheon Jun and Sang-Jun Lee. 2011. Allele-specific pcr genotyping of the hsp70 gene polymorphism discriminating the green and red color variants sea cucumber (apostichopus japonicus). Journal of genetics and genomics 38(8): 351-355. https://doi.org/10.1016/j.jgg.2011.06.002
  15. Katherine L Dunn, Paula S Espino, Bojan Drobic, Shihua He and James R Davie. 2005. The ras-mapk signal transduction pathway, cancer and chromatin remodeling. Biochemistry and Cell Biology 83(1): 1-14. https://doi.org/10.1139/o04-121
  16. Kyung-Uk Park, Jae-Yong Kim and Kwon-Il Seo. 2009. Antioxidative and cytotoxicity activities again st human colon cancer cells exhibited by edible crude saponins from soybean cake. THE KOREAN SOCIETY OF FOOD PRESERVATION 16(5): 754-758.
  17. Laura Poillet-Perez, Gilles Despouy, Regis DelageMourroux and Michael Boyer-Guittaut M. 2015. Interplay between ros and autophagy in cancer cells, from tumor initiation to cancer therapy. Redox biology 4 184-192. https://doi.org/10.1016/j.redox.2014.12.003
  18. Li L and Li Q. 2010. Effects of stocking density, temperature, and salinity on larval survival and growth of the red race of the sea cucumber apostichopus japonicus (selenka). Aquaculture international 18(3): 447-460. https://doi.org/10.1007/s10499-009-9256-4
  19. MAnami Kan-No and Akihiro Kijima. 2003. Genetic differentiation among three color variants of japanese sea cucumber stichopus japonicus. Fisheries science 69(4): 806-812. https://doi.org/10.1046/j.1444-2906.2003.00690.x
  20. Nahed El-Najjar, Manal Chatila, Hiba Moukadem, Heikki Vuorela, Matthias Ocker, Muktheshwar Gandesiri, Regine Schneider-Stock and Hala Gali-Muht asib.2010. Reactive oxygen species mediate thymoquinone-induced apoptosis and activate erk and jnk signaling. Apoptosis 15(2): 183-195. https://doi.org/10.1007/s10495-009-0421-z
  21. Naveena B. Janakiram, Altaf Mohammed and Chinthalapally V. Rao. 2015. Sea cucumbers metabolites as potent anti-cancer agents. Marine drugs 13(5): 2909-2923. https://doi.org/10.3390/md13052909
  22. Paul D. Ray, Bo-Wen Huang and Yoshiaki Tsuji. 2012. Reactive oxygen species (ros) homeostasis and redox regulation in cellular signaling. Cellular signalling 24(5): 981-990. https://doi.org/10.1016/j.cellsig.2012.01.008
  23. Pawson DL. 1980. Holothuroidea. Studies in Geology, Notes for a Short Course 3(175-189.
  24. Ryan B. Corcoran, Hiromichi Ebi, Alexa B. Turke, Erin M. Coffee, Michya Nishino, Alexandria P. Cogdill, Ronald D. Brown, Patricia Della Pelle, Dora Dias-Santagata and Kenneth E. Hung, Keith T. Flaherty, Adriano piris, Jennifer A wargo, Jeffrey Settleman, Mari Mino-Kenudson and Jeffrey A. Engelman. 2012. Egfr-mediated re-activation of mapk signaling contributes to insensitivity of braf mutant colorectal cancers to raf inhibition with vemurafenib. Cancer discovery: CD-11-0341.
  25. Saito M, Kunisaki N, Urano N and Kimura. 2002. Collagen as the major edible component of sea cucumber (stichopus japonicus). Journal of food science 67(4): 1319-1322. https://doi.org/10.1111/j.1365-2621.2002.tb10281.x
  26. Samir Attoub, Kholoud Arafat, Tamam Khalaf, Shahrazad Sulaiman and Rabah Iratni. 2018. Frondoside A Enhances the anti-cancer effects of oxaliplatin and 5-Fluorouracil on colon cancer cells. Nutrients 10(5). 560. https://doi.org/10.3390/nu10050560
  27. Sara Bordbar, Farooq Anwar and Nazamid Saari. 2011. High-value components and bioactives from sea cucumbers for functional foods-a review. Marine drugs 9(10): 1761-1805. https://doi.org/10.3390/md9101761
  28. Shan Deng, Bing Hu, Hong-Mei An, Qin Du, Ling Xu, Ke-Ping Shen, Xiu-Feng Shi, Meng-Meng Wei and Yang Wu. 2013. Teng-long-bu-zhong-tang, a chinese herbal formula, enhances anticancer effects of 5-fluorouracil in ct26 colon carcinoma. BMC complementary and alternative medicine 13(1): 128. https://doi.org/10.1186/1472-6882-13-128
  29. Shiguo Chen, Changhu Xue, Liang Yin, Qingjuan Tang, Guangli Yu and Wengang Chai. 2011. Comparison of structures and anticoagulant activities of fucosylated chondroitin sulfates from different sea cucumbers. Carbohydrate Polymers 83(2): 688-696. https://doi.org/10.1016/j.carbpol.2010.08.040
  30. Shin-Hwar Wu, Liang-Wen Hang, Jai-Sing Yang, Hung-Yi Chen, Hui-Yi Lin, Jo-Hua Chiang, Chi-Cheng Lu, Jiun-Long Yang, Tung-Yuan Lai, Yang-Ching Ko and Jing-Gung Chung. 2010. Curcumin induces apoptosis in human non-small cell lung cancer nci-h460 cells through er stress and caspase cascade-and mitochondria-dependent pathways. Anticancer research 30(6): 2125-2133.
  31. Siran Yu, Xuewei Ye, Lu Chen, Xin Xie, Qian Zhou, Xiao-Yuan Lian and Zhizhen Zhang. 2015. Cytotoxic and anti-colorectal tumor effects of sulfated saponins from sea cucumber holothuria moebii. Phytomedicine 22(12): 1112-1119. https://doi.org/10.1016/j.phymed.2015.08.007
  32. U von Freeden-Jeffry, P Vieira, L A Lucian, T McNeil, S E Burdach and R Murray. 1995. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies iL-7 as a nonredundant cytokine. Journal of Experimental Medicine 181(4): 1519-1526. https://doi.org/10.1084/jem.181.4.1519
  33. Xiao-Fang Che, Shota Moriya, Chun-Lei Zheng, Akihisa Abe, Akio Tomoda and Keisuke Miyazawa. 2013. 2-aminophenoxazine-3-one-induced apoptosis via generation of reactive oxygen species followed by c-jun n-terminal kinase activation in the human glioblastoma cell line ln229. International journal of oncology 43(5): 1456-1466. https://doi.org/10.3892/ijo.2013.2088